Showing papers in "Integrative and Comparative Biology in 2011"

Thermal Performance Curves, Phenotypic Plasticity, and the Time Scales of Temperature Exposure

Abstract: Thermal performance curves (TPCs) describe the effects of temperature on biological rate processes. Here, we use examples from our work on common killifish (Fundulus heteroclitus) to illustrate some important conceptual issues relating to TPCs in the context of using these curves to predict the responses of organisms to climate change. Phenotypic plasticity has the capacity to alter the shape and position of the TPCs for acute exposures, but these changes can be obscured when rate processes are measured only following chronic exposures. For example, the acute TPC for mitochondrial respiration in killifish is exponential in shape, but this shape changes with acclimation. If respiration rate is measured only at the acclimation temperature, the TPC is linear, concealing the underlying mechanistic complexity at an acute time scale. These issues are particularly problematic when attempting to use TPCs to predict the responses of organisms to temperature change in natural environments. Many TPCs are generated using laboratory exposures to constant temperatures, but temperature fluctuates in the natural environment, and the mechanisms influencing performance at acute and chronic time scales, and the responses of the performance traits at these time scales may be quite different. Unfortunately, our current understanding of the mechanisms underlying the responses of organisms to temperature change is incomplete, particularly with respect to integrating from processes occurring at the level of single proteins up to whole-organism functions across different time scales, which is a challenge for the development of strongly grounded mechanistic models of responses to global climate change.

Complex life cycles and the responses of insects to climate change.

Abstract: Many organisms have complex life cycles with distinct life stages that experience different environmental conditions. How does the complexity of life cycles affect the ecological and evolutionary responses of organisms to climate change? We address this question by exploring several recent case studies and synthetic analyses of insects. First, different life stages may inhabit different microhabitats, and may differ in their thermal sensitivities and other traits that are important for responses to climate. For example, the life stages of Manduca experience different patterns of thermal and hydric variability, and differ in tolerance to high temperatures. Second, life stages may differ in their mechanisms for adaptation to local climatic conditions. For example, in Colias, larvae in different geographic populations and species adapt to local climate via differences in optimal and maximal temperatures for feeding and growth, whereas adults adapt via differences in melanin of the wings and in other morphological traits. Third, we extend a recent analysis of the temperature-dependence of insect population growth to demonstrate how changes in temperature can differently impact juvenile survival and adult reproduction. In both temperate and tropical regions, high rates of adult reproduction in a given environment may not be realized if occasional, high temperatures prevent survival to maturity. This suggests that considering the differing responses of multiple life stages is essential to understand the ecological and evolutionary consequences of climate change.

The World Is not Flat: Defining Relevant Thermal Landscapes in the Context of Climate Change

Abstract: Although climates are rapidly changing on a global scale, these changes cannot easily be extrapolated to the local scales experienced by organisms. In fact, such generalizations might be quite problematic. For instance, models used to predict shifts in the ranges of species during climate change rarely incorporate data resolved to <1 km(2), although most organisms integrate climatic drivers at much smaller scales. Empirical studies alone suggest that the operative temperatures of many organisms vary by as much as 10-20 °C on a local scale, depending on vegetation, geology, and topography. Furthermore, this variation in abiotic factors ignores thermoregulatory behaviors that many animals use to balance heat loads. Through a set of simulations, we demonstrate how variability in elevational topography can attenuate the effects of warming climates. These simulations suggest that changing climates do not always impact organisms negatively. Importantly, these simulations involve well-known relationships in biophysical ecology that show how no two organisms experience the same climate in the same way. We suggest that, when coupled with thermoregulatory behavior, variation in topographic features can mask the acute effect of climate change in many cases.

The Tubercles on Humpback Whales' Flippers: Application of Bio-Inspired Technology

Abstract: : The humpback whale (Megaptera novaeangliae) is exceptional among the large baleen whales in its ability to undertake aquabatic maneuvers to catch prey. Humpback whales utilize extremely mobile, wing-like flippers for banking and turning. Large rounded tubercles along the leading edge of the flipper are morphological structures that are unique in nature. The tubercles on the leading edge act as passive-flow control devices that improve performance and maneuverability of the flipper. Experimental analysis of finite wing models has demonstrated that the presence of tubercles produces a delay in the angle of attack until stall, thereby increasing maximum lift and decreasing drag. Possible fluid-dynamic mechanisms for improved performance include delay of stall through generation of a vortex and modification of the boundary layer, and increase in effective span by reduction of both spanwise flow and strength of the tip vortex. The tubercles provide a bio-inspired design that has commercial viability for wing-like structures. Control of passive flow has the advantages of eliminating complex, costly, high-maintenance, and heavy control mechanisms, while improving performance for lifting bodies in air and water. The tubercles on the leading edge can be applied to the design of watercraft, aircraft, ventilation fans, and windmills.

Adaptive thermoregulation in endotherms may alter responses to climate change.

Abstract: Climate change is one of the major issues facing natural populations and thus a focus of recent research has been to predict the responses of organisms to these changes. Models are becoming more complex and now commonly include physiological traits of the organisms of interest. However, endothermic species have received less attention than have ectotherms in these mechanistic models. Further, it is not clear whether responses of endotherms to climate change are modified by variation in thermoregulatory characteristics associated with phenotypic plasticity and/or adaptation to past selective pressures. Here, we review the empirical data on thermal adaptation and acclimatization in endotherms and discuss how those factors may be important in models of responses to climate change. We begin with a discussion of why thermoregulation and thermal sensitivity at high body temperatures should be co-adapted. Importantly, we show that there is, in fact, considerable variation in the ability of endotherms to tolerate high body temperatures and/or high environmental temperatures, but a better understanding of this variation will likely be critical for predicting responses to future climatic scenarios. Next, we discuss why variation in thermoregulatory characteristics should be considered when modeling the effects of climate change on heterothermic endotherms. Finally, we review some biophysical and biochemical factors that will limit adaptation and acclimation in endotherms. We consider both long-term, directional climate change and short-term (but increasingly common) anomalies in climate such as extreme heat waves and we suggest areas of important future research relating to both our basic understanding of endothermic thermoregulation and the responses of endotherms to climate change.

Amphibian immune defenses against chytridiomycosis: impacts of changing environments.

Abstract: Eco-immunology is the field of study that attempts to understand the functions of the immune system in the context of the host's environment. Amphibians are currently suffering devastating declines and extinctions in nearly all parts of the world due to the emerging infectious disease chytridiomycosis caused by the chytrid fungus, Batrachochytrium dendrobatidis. Because chytridiomycosis is a skin infection and remains confined to the skin, immune defenses of the skin are critical for survival. Skin defenses include secreted antimicrobial peptides and immunoglobulins as well as antifungal metabolites produced by symbiotic skin bacteria. Low temperatures, toxic chemicals, and stress inhibit the immune system and may impair natural defenses against B. dendrobatidis. Tadpoles' mouth parts can be infected by B. dendrobatidis. Damage to the mouth parts can impair growth, and the affected tadpoles maintain the pathogen in the environment even when adults have dispersed. Newly metamorphosing frogs appear to be especially vulnerable to infection and to the lethal effects of this pathogen because the immune system undergoes a dramatic reorganization at metamorphosis, and postmetamorphic defenses are not yet mature. Here we review our current understanding of amphibian immune defenses against B. dendrobatidis and the ability of the pathogen to resist those defenses. We also briefly review what is known about the impacts of temperature, environmental chemicals, and stress on the host-pathogen interactions and suggest future directions for research.

How Nemo Finds Home: The Neuroecology of Dispersal and of Population Connectivity in Larvae of Marine Fishes

Abstract: Nearly all demersal teleost marine fishes have pelagic larval stages lasting from several days to several weeks, during which time they are subject to dispersal. Fish larvae have considerable swimming abilities, and swim in an oriented manner in the sea. Thus, they can influence their dispersal and thereby, the connectivity of their populations. However, the sensory cues marine fish larvae use for orientation in the pelagic environment remain unclear. We review current understanding of these cues and how sensory abilities of larvae develop and are used to achieve orientation with particular emphasis on coral-reef fishes. The use of sound is best understood; it travels well underwater with little attenuation, and is current-independent but location-dependent, so species that primarily utilize sound for orientation will have location-dependent orientation. Larvae of many species and families can hear over a range of ~100–1000 Hz, and can distinguish among sounds. They can localize sources of sounds, but the means by which they do so is unclear. Larvae can hear during much of their pelagic larval phase, and ontogenetically, hearing sensitivity, and frequency range improve dramatically. Species differ in sensitivity to sound and in the rate of improvement in hearing during ontogeny. Due to large differences among-species within families, no significant differences in hearing sensitivity among families have been identified. Thus, distances over which larvae can detect a given sound vary among species and greatly increase ontogenetically. Olfactory cues are current-dependent and location-dependent, so species that primarily utilize olfactory cues will have location-dependent orientation, but must be able to swim upstream to locate sources of odor. Larvae can detect odors (e.g., predators, conspecifics), during most of their pelagic phase, and at least on small scales, can localize sources of odors in shallow water, although whether they can do this in pelagic environments is unknown. Little is known of the ontogeny of olfactory ability or the range over which larvae can localize sources of odors. Imprinting on an odor has been shown in one species of reef-fish. Celestial cues are current- and location-independent, so species that primarily utilize them will have location-independent orientation that can apply over broad scales. Use of sun compass or polarized light for orientation by fish larvae is implied by some behaviors, but has not been proven. Use of neither magnetic fields nor direction of waves for orientation has been shown in marine fish larvae. We highlight research priorities in this area.

Hormone levels predict individual differences in reproductive success in a passerine bird

Abstract: Hormones mediate major physiological and behavioural components of the reproductive phenotype of individuals. To understand basic evolutionary processes in the hormonal regulation of reproductive traits, we need to know whether, and during which reproductive phases, individual variation in hormone concentrations relates to fitness in natural populations. We related circulating concentrations of prolactin and corticosterone to parental behaviour and reproductive success during both the pre-breeding and the chick-rearing stages in both individuals of pairs of free-living house sparrows, Passer domesticus. Prolactin and baseline corticosterone concentrations in pre-breeding females, and prolactin concentrations in pre-breeding males, predicted total number of fledglings. When the strong effect of lay date on total fledgling number was corrected for, only pre-breeding baseline corticosterone, but not prolactin, was negatively correlated with the reproductive success of females. During the breeding season, nestling provisioning rates of both sexes were negatively correlated with stress-induced corticosterone levels. Lastly, individuals of both sexes with low baseline corticosterone before and high baseline corticosterone during breeding raised the most offspring, suggesting that either the plasticity of this trait contributes to reproductive success or that high parental effort leads to increased hormone concentrations. Thus hormone concentrations both before and during breeding, as well as their seasonal dynamics, predict reproductive success, suggesting that individual variation in absolute concentrations and in plasticity is functionally significant, and, if heritable, may be a target of selection.

An Integrated Multi-Disciplinary Approach for Studying Multiple Stressors in Freshwater Ecosystems: Daphnia as a Model Organism

Abstract: Synopsis The increased overexploitation of freshwater ecosystems and their extended watersheds often generates a cascade of anthropogenic stressors (e.g., acidification, eutrophication, metal contamination, Ca decline, changes in the physical environment, introduction of invasive species, over-harvesting of resources). The combined effect of these stressors is particularly difficult to study, requiring a coordinated multi-disciplinary effort and insights from various sub-disciplines of biology, including ecology, evolution, toxicology, and genetics. It also would benefit from a welldeveloped and broadly accepted model systems. The freshwater crustacean Daphnia is an excellent model organism for studying multiple stressors because it has been a chosen focus of study in all four of these fields. Daphnia is a widespread keystone species in most freshwater ecosystems, where it is routinely exposed to a multitude of anthropogenic and natural stressors. It has a fully sequenced genome, a well-understood life history and ecology, and a huge library of responses to toxicity. To make the case for its value as a model species, we consider the joint and separate effects of natural and three anthropogenic stressors—climatic change, calcium decline, and metal contaminants on daphniids. We propose that integrative approaches marrying various subfields of biology can advance our understanding of the combined effects of stressors. Such approaches can involve the measuring of multiple responses at several levels of biological organization from molecules to natural populations. For example, novel interdisciplinary approaches such as transcriptome profiling and mutation accumulation experiments can offer insights into how multiple stressors influence gene transcription and mutation rates across genomes, and, thus, help determine the causal mechanism between environmental stressors and population/community effects as well as long-term evolutionary patterns.

From Host Immunity to Pathogen Invasion: The Effects of Helminth Coinfection on the Dynamics of Microparasites

Abstract: Concurrent infections with multiple parasites are ubiquitous in nature. Coinfecting parasites can interact with one another in a variety of ways, including through the host's immune system via mechanisms such as immune trade-offs and immunosuppression. These within-host immune processes mediating interactions among parasites have been described in detail, but how they scale up to determine disease dynamic patterns at the population level is only beginning to be explored. In this review, we use helminth-microparasite coinfection as a model for examining how within-host immunological effects may influence the ecological outcome of microparasitic diseases, with a specific focus on disease invasion. The current literature on coinfection between helminths and major microparasitic diseases includes many studies documenting the effects of helminths on individual host responses to microparasites. In many cases, the observed host responses map directly onto parameters relevant for quantifying disease dynamics; however, there have been few attempts at integrating data on individual-level effects into theoretical models to extrapolate from the individual to the population level. Moreover, there is considerable variability in the particular combination of disease parameters affected by helminths across different microparasite systems. We develop a conceptual framework identifying some potential sources of such variability: Pathogen persistence and severity, and resource availability to hosts. We also generate testable hypotheses regarding diseases and the environmental contexts when the effects of helminths on microparasite dynamics should be most pronounced. Finally, we use a case study of helminth and mycobacterial coinfection in the African buffalo to illustrate both progress and challenges in understanding the population-level consequences of within-host immunological interactions, and conclude with suggestions for future research that will help improve our understanding of the effects of coinfection on dynamics of infectious diseases.

Environmentally cued hatching across taxa: embryos respond to risk and opportunity.

Abstract: Most animals begin life in eggs, protected and constrained by a capsule, shell, or other barrier. As embryos develop, their needs and abilities change, altering the costs and benefits of encapsulation, and the risks and opportunities of the outside world. When the cost/benefit ratio is better outside the egg, animals should hatch. Adaptive timing of hatching evolves in this context. However, many environmental variables affect the optimal timing of hatching so there is often no consistent best time. Across a broad range of animals, from flatworms and snails to frogs and birds, embryos hatch at different times or at different developmental stages in response to changing risks or opportunities. Embryos respond to many types of cues, assessed via different sensory modalities. Some responses appear simple. Others are surprisingly complex and sophisticated. Parents also manipulate the timing of hatching. The number and breadth of examples of cued hatching suggest that, in the absence of specific information, we should not assume that hatching timing is fixed. Our challenge now is to integrate information on the timing of hatching across taxa to better understand the diversity of patterns and how they are structured in relation to different types of environmental and developmental variation. As starting points for comparative studies, I: (1) suggest a framework based on heterokairy-individual, plastic variation in the rate, timing, or sequence of developmental events and processes-to describe patterns and mechanisms of variation in the timing of hatching; (2) briefly review the distribution of environmentally cued hatching across the three major clades of Bilateria, highlighting the diverse environmental factors and mechanisms involved; and (3) discuss factors that shape the diversity of plastic and fixed timing of hatching, drawing on evolutionary theory on phenotypic plasticity which directs our attention to fitness trade-offs, environmental heterogeneity, and predictive cues. Combining mechanistic and evolutionary perspectives is necessary because development changes organismal interactions with the environment. Integrative and comparative studies of the timing of hatching will improve our understanding of embryos as both evolving and developing organisms.

Plasticity of hatching in amphibians: evolution, trade-offs, cues and mechanisms

Abstract: Many species of frogs and salamanders, in at least 12 families, alter their timing of hatching in response to conditions affecting mortality of eggs or larvae. Some terrestrially laid or stranded embryos wait to hatch until they are submerged in water. Some embryos laid above water accelerate hatching if the eggs are dehydrating; others hatch early if flooded. Embryos can hatch early in response to predators and pathogens of eggs or delay hatching in response to predators of larvae; some species do both. The phylogenetic pattern of environmentally cued hatching suggests that similar responses have evolved convergently in multiple amphibian lineages. The use of similar cues, including hypoxia and physical disturbance, in multiple contexts suggests potential shared mechanisms underlying the capacity of embryos to respond to environmental conditions. Shifts in the timing of hatching often have clear benefits, but we know less about the trade-offs that favor plasticity, the mechanisms that enable it, and its evolutionary history. Some potentially important types of cued hatching, such as those involving embryo-parent interactions, are relatively unexplored. I discuss promising directions for research and the opportunities that the hatching of amphibians offers for integrative studies of the mechanisms, ecology and evolution of a critical transition between life-history stages.

Evaporative Water Loss Is a Plausible Explanation for Mortality of Bats from White-Nose Syndrome

Abstract: Synopsis White-nose syndrome (WNS) has caused alarming declines of North American bat populations in the 5 years since its discovery. Affected bats appear to starve during hibernation, possibly because of disruption of normal cycles of torpor and arousal. The importance of hydration state and evaporative water loss (EWL) for influencing the duration of torpor bouts in hibernating mammals recently led to ‘‘the dehydration hypothesis,’’ that cutaneous infection of the wing membranes of bats with the fungus Geomyces destructans causes dehydration which in turn, increases arousal frequency during hibernation. This hypothesis predicts that uninfected individuals of species most susceptible to WNS, like little brown bats (Myotis lucifugus), exhibit high rates of EWL compared to less susceptible species. We tested the feasibility of this prediction using data from the literature and new data quantifying EWL in Natterer’s bats (Myotis nattereri), a species that is, like other European bats, sympatric with G. destructans but does not appear to suffer significant mortality from WNS. We found that little brown bats exhibited significantly higher rates of normothermic EWL than did other bat species for which comparable EWL data are available. We also found that Natterer’s bats exhibited significantly lower rates of EWL, in both wet and dry air, compared with values predicted for little brown bats exposed to identical relative humidity (RH). We used a population model to show that the increase in EWL required to cause the pattern of mortality observed for WNS-affected little brown bats was small, equivalent to a solitary bat hibernating exposed to RH of � 95%, or clusters hibernating in � 87% RH, as opposed to typical near-saturation conditions. Both of these results suggest the dehydration hypothesis is plausible and worth pursuing as a possible explanation for mortality of bats from WNS.

Does animal behavior underlie covariation between hosts' exposure to infectious agents and susceptibility to infection? Implications for disease dynamics.

Abstract: Animal behavior is unique in influencing both components of the process of transmission of disease: exposure to infectious agents, and susceptibility to infection once exposed. To date, the influence of behavior on exposure versus susceptibility has largely been considered separately. Here, we ask whether these two key mechanisms act in concert in natural populations, whereby individuals who are most exposed to infectious agents or have the most contact with conspecifics are also the most susceptible or infectious. We propose three mechanisms that can generate covariation between these two key elements of the transmission of disease within and among hosts, and we provide empirical examples of each. We then use a mathematical model to examine the effect of this covariation on the dynamics of disease at the population level. First, we show that the empirical mechanisms generating covariation between behavioral and physiological components of disease transmission are widespread and include endocrine mediators of behavior, mate choice, group size, sickness behaviors, and behavioral avoidance of infectious conspecifics. The diversity of these empirical mechanisms underscores the potential importance and breadth of covariation in the disease process. Second, we show mathematically that the variability in hosts' exposure to infectious agents and susceptibility or infectiousness, and how tightly they are coupled, strongly influences the ability of a disease to invade a host population. Overall, we propose that covariation between behavioral and physiological components of transmission is likely widespread in natural populations, and can have important consequences for the dynamics of disease at the population level as well as for our understanding of sexual selection, social behavior, and animal communication.

Heterothermy in Afrotropical mammals and birds: a review.

Abstract: Synopsis Recent years have seen a rapid increase in the number of Afrotropical endotherms known to avoid mismatches between energy supply and demand by using daily torpor and/or hibernation. Among mammals, heterothermy has been reported in 40 species in six orders, namely Macroscelidea, Afrosoricida, Rodentia, Eulipotyphla, Primates and Chiroptera. These species span a range in body mass of 7–770g, with minimum heterothermic body temperatures ranging from 1–278C and bout length varying from 1h to 70 days. Daily torpor is the most common form of heterothermy, with true hibernation being observed in only seven species, Graphiurus murinus, Graphiurus ocularis, Atelerix frontalis, Cheirogaleus medius, Cheirogaleus major, Microcebus murinus and Microcebus griseorufus. The traditional distinction between daily torpor and hibernation is blurred in some species, with free-ranging individuals exhibiting bouts of 424h and body temperatures 5168C, but none of the classical behaviours associated with hibernation. Several species bask in the sun during rewarming. Among birds, heterothermy has been reported in 16 species in seven orders, and is more pronounced in phylogenetically older taxa. Both in mammals and birds, patterns of heterothermy can vary dramatically among species occurring at a particular site, and even among individuals of a single species. For instance, patterns of heterothermy among cheirogalid primates in western Madagascar vary from daily torpor to uninterrupted hibernation for up to seven months. Other examples of variation among closely-related species involve small owls, elephant shrews and vespertilionid bats. There may also be variation in terms of the ecological correlates of torpor within a species, as is the case in the Freckled Nightjar Caprimulgus tristigma.

Incorporating Population-Level Variation in Thermal Performance into Predictions of Geographic Range Shifts

Abstract: Determining how species' geographic ranges are governed by current climates and how they will respond to rapid climatic change poses a major biological challenge. Geographic ranges are often spatially fragmented and composed of genetically differentiated populations that are locally adapted to different thermal regimes. Tradeoffs between different aspects of thermal performance, such as between tolerance to high temperature and tolerance to low temperature or between maximal performance and breadth of performance, suggest that the performance of a given population will be a subset of that of the species. Therefore, species-level projections of distribution might overestimate the species' ability to persist at any given location. However, current approaches to modeling distributions often do not consider variation among populations. Here, we estimated genetically-based differences in thermal performance curves for growth among 12 populations of the scarlet monkeyflower, Mimulus cardinalis, a perennial herb of western North America. We inferred the maximum relative growth rate (RGR(max)), temperature optimum (T(opt)), and temperature breadth (T(breadth)) for each population. We used these data to test for tradeoffs in thermal performance, generate mechanistic population-level projections of distribution under current and future climates, and examine how variation in aspects of thermal performance influences forecasts of range shifts. Populations differed significantly in RGR(max) and had variable, but overlapping, estimates of T(opt) and T(breadth). T(opt) declined with latitude and increased with temperature of origin, consistent with tradeoffs between performances at low temperatures versus those at high temperatures. Further, T(breadth) was negatively related to RGR(max), as expected for a specialist-generalist tradeoff. Parameters of the thermal performance curve influenced properties of projected distributions. For both current and future climates, T(opt) was negatively related to latitudinal position, while T(breadth) was positively related to projected range size. The magnitude and direction of range shifts also varied with T(opt) and T(breadth), but sometimes in unexpected ways. For example, the fraction of habitat remaining suitable increased with T(opt) but decreased with T(breadth). Northern limits of all populations were projected to shift north, but the magnitude of shift decreased with T(opt) and increased with T(breadth). Median latitude was projected to shift north for populations with high T(breadth) and low T(opt), but south for populations with low T(breadth) and high T(opt). Distributions inferred by integrating population-level projections did not differ from a species-level projection that ignored variation among populations. However, the species-level approach masked the potential array of divergent responses by populations that might lead to genotypic sorting within the species' range. Thermal performance tradeoffs among populations within the species' range had important, but sometimes counterintuitive, effects on projected responses to climatic change.

Hibernation and torpor in tropical and subtropical bats in relation to energetics, extinctions, and the evolution of endothermy.

Abstract: Torpor, the most effective means of energy conservation available to endotherms, is still widely viewed as a specific adaptation in a few high-latitude, cold-climate endotherms with no adaptive function in warm regions. Nevertheless, a growing number of diverse terrestrial mammals and birds from low latitudes (0-30°), including species from tropical and subtropical regions, are heterothermic and employ torpor. Use of torpor is especially important for bats because they are small, expend large amounts of energy when active, rely on a fluctuating food supply, and have only a limited capacity for storage of fat. Patterns of torpor in tropical/subtropical bats are highly variable, but short bouts of torpor with relatively high body temperatures (T(b)) are most common. Hibernation (a sequence of multiday bouts of torpor) has been reported for free-ranging subtropical tree-dwelling vespertilionids, cave-dwelling hipposiderids, and house-dwelling molossids. The observed range of minimum T(b) is ∼6-30 °C, and the reduction of energy expenditure through the use of torpor, in comparison to normothermic values, ranges from 50 to 99%. Overall, torpor in the tropics/subtropics has been reported for 10 out of the currently recognized 18 bat families, which contain 1079 species, or 96.7% of all bats. Although it is unlikely that all of these are heterothermic, the large majority probably will be. Frequent use of torpor, including hibernation in diverse groups of tropical/subtropical bats, suggests that heterothermy is an ancestral chiropteran trait. Although data especially from the field are still scarce, it is likely that torpor, highly effective in reducing requirements for energy and water even under warm conditions, plays a crucial role in the long-term survival of the majority of small tropical and subtropical bats. Discovering how bats achieve this provides numerous opportunities for exiting new research.

Effect of Flexural and Torsional Wing Flexibility on Lift Generation in Hoverfly Flight

Abstract: Synopsis The effect of wing flexibility in hoverflies was investigated using an at-scale mechanical model. Unlike dynamically-scaled models, an at-scale model can include all phenomena related to motion and deformation of the wing during flapping. For this purpose, an at-scale polymer wing mimicking a hoverfly was fabricated using a custom micromolding process. The wing has venation and corrugation profiles which mimic those of a hoverfly wing and the measured flexural stiffness of the artificial wing is comparable to that of the natural wing. To emulate the torsional flexibility at the wing-body joint, a discrete flexure hinge was created. A range of flexure stiffnesses was chosen to match the torsional stiffness of pronation and supination in a hoverfly wing. The polymer wing was compared with a rigid, flat, carbon-fiber wing using a flapping mechanism driven by a piezoelectric actuator. Both wings exhibited passive rotation around the wing hinge; however, these rotations were reduced in the case of the compliant polymer wing due to chordwise deformations during flapping which caused a reduced effective angle of attack. Maximum lift was achieved when the stiffness of the hinge was similar to that of a hoverfly in both wing cases and the magnitude of measured lift is sufficient for hovering; the maximum lift achieved by the single polymer and carbon-fiber wings was 5.9 � 10 2 mN and 6.9 � 10 2 mN, respectively. These results suggest that hoverflies could exploit intrinsic compliances to generate desired motions of the wing and that, for the same flapping motions, a rigid wing could be more suitable for producing large lift.

Aerial Righting Reflexes in Flightless Animals

Abstract: Synopsis Animals that fall upside down typically engage in an aerial righting response so as to reorient dorsoventrally. This behavior can be preparatory to gliding or other controlled aerial behaviors and is ultimately necessary for a successful landing. Aerial righting reflexes have been described historically in various mammals such as cats, guinea pigs, rabbits, rats, and primates. The mechanisms whereby such righting can be accomplished depend on the size of the animal and on anatomical features associated with motion of the limbs and body. Here we apply a comparative approach to the study of aerial righting to explore the diverse strategies used for reorientation in midair. We discuss data for two species of lizards, the gecko Hemidactylus platyurus and the anole Anolis carolinensis, as well as for the first instar of the stick insect Extatosoma tiaratum, to illustrate size-dependence of this phenomenon and its relevance to subsequent aerial performance in parachuting and gliding animals. Geckos can use rotation of their large tails to reorient their bodies via conservation of angular momentum. Lizards with tails well exceeding snout-vent length, and correspondingly large tail inertia to body inertia ratios, are more effective at creating midair reorientation maneuvers. Moreover, experiments with stick insects, weighing an order of magnitude less than the lizards, suggest that aerodynamic torques acting on the limbs and body may play a dominant role in the righting process for small invertebrates. Both inertial and aerodynamic effects, therefore, can play a role in the control of aerial righting. We propose that aerial righting reflexes are widespread among arboreal vertebrates and arthropods and that they represent an important initial adaptation in the evolution of controlled aerial behavior.

Heat for Nothing or Activity for Free? Evidence and Implications of Activity-Thermoregulatory Heat Substitution

Abstract: If heat generated through activity can substitute for heat required for thermoregulation, then activity in cold environments may be energetically free for endotherms. Although the possibility of activity-thermoregulatory heat substitution has been long recognized, its empirical generality and ecological implications remain unclear. We combine a review of the literature and a model of heat exchange to explore the generality of activity-thermoregulatory heat substitution, to assess the extent to which substitution is likely to vary with body size and ambient temperature, and to examine some potential macroecological implications. A majority of the 51 studies we located showed evidence of activity-thermoregulatory heat substitution (35 of 51 studies), with 28 of 32 species examined characterized by substitution in one or more study. Among studies that did detect substitution, the average magnitude of substitution was 57%, but its occurrence and extent varied taxonomically, allometrically, and with ambient temperature. Modeling of heat production and dissipation suggests that large birds and mammals, engaged in intense activity and exposed to relatively warm conditions, have more scope for substitution than do smaller endotherms engaged in less intense activity and experiencing cooler conditions. However, ambient temperature has to be less than the lower critical temperature (the lower bound of the thermal neutral zone) for activity-thermoregulatory heat substitution to occur and this threshold is lower in large endotherms than in small endotherms. Thus, in nature, substitution is most likely to be observed in intermediate-sized birds and mammals experiencing intermediate ambient temperatures. Activity-thermoregulatory heat substitution may be an important determinant of the activity patterns and metabolic ecology of endotherms. For example, a pattern of widely varying field metabolic rates (FMR) at low latitudes that converges to higher and less variable FMR at high latitudes has been interpreted as suggesting that warm environments at low latitudes allow a greater variety of feasible metabolic niches than do cool, high-latitude environments. However, activity-thermoregulatory heat substitution will generate this pattern of latitudinal FMR variation even if endotherms from cold and warm climates are metabolically and behaviorally identical, because the metabolic rates of resting and active animals are more similar in cold than in warm environments. Activity-thermoregulatory heat substitution is an understudied aspect of endotherm thermal biology that is apt to be a major influence on the physiological, behavioral and ecological responses of free-ranging endotherms to variation in temperature.

Animal Aloft: The Origins of Aerial Behavior and Flight

Abstract: Diverse taxa of animals exhibit remarkable aerial capacities, including jumping, mid-air righting, parachuting, gliding, landing, controlled maneuvers, and flapping flight. The origin of flapping wings in hexapods and in 3 separate lineages of vertebrates (pterosaurs, bats, and birds) greatly facilitated subsequent diversification of lineages, but both the paleobiological context and the possible selective pressures for the evolution of wings remain contentious. Larvae of various arboreal hemimetabolous insects, as well as many adult canopy ants, demonstrate the capacity for directed aerial descent in the absence of wings. Aerial control in the ancestrally wingless archaeognathans suggests that flight behavior preceded the origins of wings in hexapods. In evolutionary terms, the use of winglets and partial wings to effect aerial righting and maneuvers could select for enhanced appendicular motions, and ultimately lead to powered flight. Flight behaviors that involve neither flapping nor wings are likely to be much more widespread than is currently recognized. Further characterization of the sensory and biomechanical mechanisms used by these aerially capable taxa can potentially assist in reconstruction of ancestral winged morphologies and facilitate our understanding of the origins of flight.

Environmentally cued hatching in reptiles.

Abstract: Evidence is accumulating for the widespread occurrence of environmentally cued hatching (ECH) in animals, but its diversity and distribution across taxa are unknown. Herein I review three types of ECH in reptiles: early hatching, delayed hatching, and synchronous hatching. ECH is currently known from 43 species, including turtles, crocodilians, lizards, snakes, tuatara, and possibly worm lizards. Early hatching caused by physical disturbance (e.g., vibrations) is the most commonly reported ECH across all groups; although it apparently serves an antipredator function in some species, its adaptive value is unknown in most. Delayed hatching, characterized by metabolic depression or embryonic aestivation, and sometimes followed by a hypoxic cue (flooding), occurs in some turtles and possibly in monitor lizards and crocodilians; in some of these species delayed hatching serves to defer hatching from the dry season until the more favorable conditions of the wet season. Synchronous hatching, whereby sibling eggs hatch synchronously despite vertical thermal gradients in the nest, occurs in some turtles and crocodilians. Although vibrations and vocalizations in hatching-competent embryos can stimulate synchronous hatching, cues promoting developmentally less advanced embryos to catch up with more advanced embryos have not been confirmed. Synchronous hatching may serve to dilute predation risk by promoting synchronous emergence or reduce the period in which smells associated with hatching can attract predators to unhatched eggs. Within species, advancing our understanding of ECH requires three types of studies: (1) experiments identifying hatching cues and the plastic hatching period, (2) experiments disentangling hypotheses about multiple hatching cues, and (3) investigations into the environmental context in which ECH might evolve in different species (major predators or abiotic influences on the egg, embryo, and hatchling). Among species and groups, surveys for ECH are required to understand its evolutionary history in reptiles. The probability of ECH occurring is likely influenced by a species's life history, ecology, behavior, and interrelationships with other species (e.g., sizes of predator and prey). More broadly, the discovery of embryo-embryo communication as a mechanism for synchronous hatching in crocodilians and turtles indicates that the social behavior of (nonavian) reptiles has been underestimated.

Timing of Hatching and Release of Larvae by Brachyuran Crabs: Patterns, Adaptive Significance and Control

Abstract: Most semiterrestrial, intertidal and shallow subtidal brachyuran crabs that live in tropical and warm temperate estuaries, bays and protected coasts world-wide release their planktonic larvae near the times of nocturnal high tides on the larger amplitude tides in the biweekly or monthly cycles of tidal amplitude. Crab larvae usually emigrate quickly to the sea where they develop to return as postlarvae to settle in habitats suitable for their survival. Predators of larvae are more abundant where larvae are released than where they develop, suggesting that this migration from estuaries to the sea reduces predation on larvae. Crabs with larvae that are relatively well-protected by spines and cryptic colors do not emigrate and often lack strong reproductive cycles, lending support to this explanation. Adults control the timing of the release of larvae with respect to the biweekly and monthly cycles of tidal amplitude by controlling when they court and mate and females control when development begins by controlling when they ovulate and allow their eggs to be fertilized by stored sperm. By changing the time they breed, fiddler crabs (Uca terpsichores) compensate for the effects of spatial and temporal variation in incubation temperature on development rates so that embryos are ready to hatch at the appropriate time. Control of the diel and tidal timing of hatching and of release of larvae varies with where adults live. Females of the more terrestrial species often move from protected incubation sites, sometimes far from water, and they largely control the precise time, both, of hatching and of release of larvae. Females of intertidal species also may influence when embryos begin to hatch. Upon hatching, a chemical cue is released that stimulates the female to pump her abdomen, causing rapid hatching and release of all larvae in her clutch. Embryos, rather than females, largely control hatching in subtidal species, perhaps because females incubate their eggs where they release their larvae. Topics for further study include the mechanism whereby adults regulate the timing of breeding, the mechanisms by which females control development rates of embryos, the nature of communication between females and embryos that leads to precise and synchronous hatching by the number (often thousands) of embryos in a clutch, and the causes of selection for such precision. The timing of hatching and of release of larvae by cold-temperate, Arctic, and Antarctic species and by fully terrestrial and freshwater tropical species has received little attention.

Pathogen Pressure Puts Immune Defense into Perspective

Abstract: The extent to which organisms can protect themselves from disease depends on both the immune defenses they maintain and the pathogens they face. At the same time, immune systems are shaped by the antigens they encounter, both over ecological and evolutionary time. Ecological immunologists often recognize these interactions, yet ecological immunology currently lacks major efforts to characterize the environmental, host-independent, antigenic pressures to which all animals are exposed. Failure to quantify relevant diseases and pathogens in studies of ecological immunology leads to contradictory hypotheses. In contrast, including measures of environmental and host-derived commensals, pathogens, and other immune-relevant organisms will strengthen the field of ecological immunology. In this article, we examine how pathogens and other organisms shape immune defenses and highlight why such information is essential for a better understanding of the causes of variation in immune defenses. We introduce the concept of "operative protection" for understanding the role of immunologically relevant organisms in shaping immune defense profiles, and demonstrate how the evolutionary implications of immune function are best understood in the context of the pressures that diseases and pathogens bring to bear on their hosts. We illustrate common mistakes in characterizing these immune-selective pressures, and provide suggestions for the use of molecular and other methods for measuring immune-relevant organisms.

Integrator Networks: Illuminating the Black Box Linking Genotype and Phenotype

Abstract: Emerging concepts in developmental biology, such as facilitated variation and dynamical patterning modules, address a major shortcoming of the Modern Synthesis in Biology: how genotypic variation is transduced into functional yet diverse phenotypic variation. Still, we lack a theory to explain how variation at the cellular and tissue level is coordinated into variation at the whole-organism level, especially as priority of cellular and tissue functions change over an individual's lifetime and are influenced by environmental variation. Here, we propose that interactions among a limited subset of physiological factors that we call, integrators, regulate most phenotypic variation at the organismal level. Integrators are unique among physiological factors in that they have the propensity to coordinate the expression of conserved gene modules of most types of tissues because they participate as nodes in a hierarchical network. In other words, integrator networks impose physiological epistasis, meaning that whole-organism phenotypic responses will be influenced by previous experiences, current environmental conditions, and fitness priorities as encoded by individual integrators. Below, we provide examples of how integrator networks are responsible for both profound and irreversible phenotypic changes (i.e., metamorphosis, sexual differentiation) as well as subtler, transient (e.g., pelage color, seasonal fluctuations in lymphoid and reproductive tissues) variation. The goal of this article is not to describe completely how integrator networks function, but to stimulate discussion about the role of physiology in linking genetic to phenotypic variation. To generate useful data sets for understanding integrator networks and to inform whole-organism physiology generally, we describe several useful tools including vector-field editing, response-surface regression, and experiments of life-table responses. We then close by highlighting some implications of integrator networks for conservation and biomedicine.

Speciation Genes in Free-Spawning Marine Invertebrates

Abstract: Synopsis Research on speciation of marine organisms has lagged behind that of terrestrial ones, but the study of the evolution of molecules involved in the adhesion of gametes in free-spawning invertebrates is an exception. Here I review the function, species-specificity, and molecular variation of loci coding for bindin in sea urchins, lysin in abalone and their egg receptors, in an effort to assess the degree to which they contribute to the emergence of reproductive isolation during the speciation process. Bindin is a protein that mediates binding of the sperm to the vitelline envelope (VE) of the egg and the fusion of the gametes’ membranes, whereas lysin is a protein involved only in binding to the VE. Both of these molecules are important in species recognition by the gametes, but they rarely constitute absolute blocks to interspecific hybridization. Intraspecific polymorphism is high in bindin, but low in lysin. Polymorphism in bindin is maintained by frequency-dependent selection due to sexual conflict arising from the danger of polyspermy under high densities of sperm. Monomorphism in lysin is the result of purifying selection arising from the need for species recognition. Interspecific divergence in lysin is due to strong positive selection, and the same is true for bindin of four out of seven genera of sea urchins studied to date. The differences between the sea urchin genera in the strength of selection can only partially be explained by the hypothesis of reinforcement. The egg receptor for lysin (VERL) is a glycoprotein with 22 repeats, 20 of which have evolved neutrally and homogenized by concerted evolution, whereas the first two repeats are under positive selection. Selection on lysin has been generated by the need to track changes in VERL, permitted by the redundant structure of this molecule. Both lysin and bindin are important in reproductive isolation, probably had a role in speciation, but it is hard to determine whether they meet the strictest criteria of ‘‘speciation loci,’’ defined as genes whose differentiation has caused speciation.

Gliding Flight in Chrysopelea: Turning a Snake into a Wing

Abstract: Although many cylindrical animals swim through water, flying snakes of the genus Chrysopelea are the only limbless animals that glide through air. Despite a lack of limbs, these snakes can actively launch by jumping, maintain a stable glide path without obvious control surfaces, maneuver, and safely land without injury. Jumping takeoffs employ vertically looped kinematics that seem to be different than any other behavior in limbless vertebrates, and their presence in a closely related genus suggests that gap-crossing may have been a behavioral precursor to the evolution of gliding in snakes. Change in shape of the body by dorsoventral flattening and high-amplitude aerial undulation comprise two key features of snakes' gliding behavior. As the snake becomes airborne, the body flattens sequentially from head to vent, forming a cross-sectional shape that is roughly triangular, with a flat surface and lateral "lips" that protrude ventrally on each side of the body; these may diminish toward the vent. This shape likely provides the snake with lift coefficients that peak at high angles of attack and gentle stall characteristics. A glide trajectory is initiated with the snake falling at a steep angle. As the snake rotates in the pitch axis, it forms a wide "S" shape and begins undulating in a complex three-dimensional pattern, with the body angled upward relative to the glide path. The head moves side-to-side, sending traveling waves posteriorly toward the tail, while the body (most prominently, the posterior end) oscillates in the vertical axis. These active movements while gliding are substantially different and more dynamic than those used by any other animal glider. As the snake gains forward speed, the glide path becomes less steep, reaching minimally recorded glide angles of 13°. In general, smaller snakes appear to be more proficient gliders. Chrysopelea paradisi can also maneuver and land either on the ground or on vegetation, but these locomotor behaviors have not been studied in detail. Future work aims to understand the mechanisms of production and control of force in takeoff, gliding, and landing, and to identify the musculoskeletal adaptations that enable this unique form of locomotion.

Population Differentiation in the Open Sea: Insights from the Pelagic Copepod Pleuromamma xiphias

Abstract: Although a number of recent studies of marine holoplankton have reported significant genetic structure among populations, little is currently known about the biological and oceanographic processes that influence population connectivity in oceanic plankton. In order to examine how depth preferences influence dispersal in oceanic plankton, I characterized the genetic structure of a copepod with diel vertical migration (DVM) (Pleuromamma xiphias), throughout its global distribution, and compared these results to those expected given the interaction of this species' habitat depth with ocean circulation and bathymetry. Mitochondrial COI sequences from 651 individuals from 28 sites in the Indian, Pacific, and Atlantic Oceans revealed highly significant genetic differentiation both within and among ocean basins. Limited dispersal among distinct pelagic provinces seems to have played a major role in population differentiation in this species, with strong genetic breaks observed across known oceanographic fronts or current systems in all three ocean basins. The Indo-West Pacific (IWP) holds a highly distinct genetic population of this species that was sampled in both the western Pacific and eastern Indian Oceans. This suggests that the IWP does not act as a strong barrier to gene flow between basins, as expected, despite the relatively shallow water depth ( 400 m) diel migration of this species. A pattern of isolation by distance was observed in the Indian Ocean with genetic differentiation among samples down to spatial scales of ∼800 km, indicating that realized dispersal in P. xiphias occurs over much smaller spatial scales than in previously reported oceanic holoplankton. Given its highly regionalized population genetic structure, P. xiphias may have some capacity to adapt to local oceanographic conditions, and it should not be assumed that populations of this species in distinct pelagic biomes will respond in the same way to shared physical or climatic forcing.

Shorebirds' Seasonal Adjustments in Thermogenic Capacity Are Reflected by Changes in Body Mass: How Preprogrammed and Instantaneous Acclimation Work Together

Abstract: Phenotypic flexibility in shorebirds has been studied mainly in the context of adjustments to migration and to quality of food; little is known on how birds adjust their phenotype to harsh winter conditions. We showed earlier that red knot (Calidris canutus islandica) can acclimate to cold by elevating body mass. This goes together with larger pectoral muscles, i.e., greater shivering machinery, and thus, better thermogenic capacity. Here, we present results of a yearlong experiment with indoor captive knots to determine whether this strategy is part of their natural seasonal phenotypic cycle. We maintained birds under three thermal regimes: constant cold (5 degrees C), constant thermoneutrality (25 degrees C) and natural seasonal variation between these extremes (9-22 degrees C). Each month we measured variables related to the birds' endurance to cold and physiological maintenance [body mass, thickness of pectoral muscles, summit metabolic rate (M(sum)), food intake, gizzard size, basal metabolic rate (BMR)]. Birds from all treatments expressed synchronized and comparable variation in body mass in spite of thermal treatments, with a 17-18% increase between the warmest and coldest months of the year; which appeared regulated by an endogenous driver. In addition, birds living in the cold exhibited a 10% higher average body mass than did those maintained at thermoneutrality. Thickness of the pectoral muscle tracked changes in body mass in all treatments and likely contributed to greater capacity for shivering in heavier birds. Consequently, M(sum) was 13% higher in cold-acclimated birds compared to those experiencing no thermoregulation costs. However, our data also suggest that part of maximal heat production comes from nonshivering processes. Birds facing cold conditions ate up to 25% more food than did birds under thermoneutral conditions, yet did not develop larger gizzards. Seasonal variation in BMR followed changes in body mass, probably reflecting changes in mass of metabolically active tissues. Just as cold-exposed birds, red knots in the variable treatment increased body mass in winter, thereby improving cold endurance. During summer, however, they maintained a lower body mass and thermogenic capacity compared to cold-exposed birds, similar to individuals kept at thermoneutrality. We conclude that red knots acclimate to seasonal variations in ambient temperature by modulating body mass, combining a preprogrammed increase in mass during winter with a capacity for fine-tuning body mass and thermogenic capacity to temperature variations.

Plasticity of hatching and the duration of planktonic development in marine invertebrates.

Abstract: Plasticity in hatching potentially adjusts risks of benthic and planktonic development for benthic marine invertebrates. The proportionate effect of hatching plasticity on duration of larval swimming is greatest for animals that can potentially brood or encapsulate offspring until hatching near metamorphic competence. As an example, early hatching of the nudibranch mollusk Phestilla sibogae is stimulated by scattering of encapsulated offspring, as by a predator feeding on the gelatinous egg ribbon. When egg ribbons are undisturbed, hatching is at or near metamorphic competence. Disturbance of an unguarded benthic egg mass can insert 4 or more days of obligate larval dispersal into the life history. As another example, the spionid annelid Boccardia proboscidea broods capsules, each with both cannibalistic and developmentally arrested planktivorous siblings plus nurse eggs. Early hatching produces mainly planktivorous larvae with a planktonic duration of 15 days. Late hatching produces mainly adelphophages who have eaten their planktivorous siblings and metamorphose with little or no period of swimming. Mothers actively hatch their offspring by tearing the capsules, and appeared to time hatching in response to their environment and not to the stage of development of their offspring. Higher temperature increased the variance of brooding time. Females appeared to hatch capsules at an earlier developmental stage at lower temperatures. Species that release gametes or zygotes directly into the plankton have less scope for plasticity in stage at hatching. Their embryos develop singly with little protection and hatch at early stages, often as blastulae or gastrulae. Time of hatching cannot be greatly advanced, and sensory capabilities of blastulae may be limited.