Spiders in motion: demonstrating adaptation, structure-function relationships, and trade-offs in invertebrates.

Evolutionary history and structural considerations constrain all aspects of animal physiology. Constraints on invertebrate locomotion are especially straightforward for students to observe and understand. In this exercise, students use spiders to investigate the concepts of adaptation, structure-function relationships, and trade-offs. Students measure burst and endurance performance in several taxonomic families of spiders whose ecological niches have led to different locomotory adaptations. Based on observations of spiders in their natural habitat and prior background information, students make predictions about spider performance. Students then construct their own knowledge by performing a hands-on, inquiry-based scientific experiment where the results are not necessarily known. Depending on the specific families chosen, students can observe that web-dwelling spiders have more difficulty navigating complex terrestrial terrain than ground-dwelling spiders and that there is a trade-off between burst performance and endurance performance in spiders. Our inexpensive runway design allows for countless variations on this basic experiment; for example, we have successfully used runways to show students how the performance of heterothermic ectotherms varies with temperature. High levels of intra- and interindividual variation in performance underscore the importance of using multiple trials and statistical tests. Finally, this laboratory activity can be completely student driven or standardized, depending on the instructor's preference.

Prior exposure to repeated morphine potentiates mechanical allodynia induced by peripheral inflammation and neuropathy.

Opioids, such as morphine, induce potent analgesia and are the gold standard for the treatment of acute pain. However, opioids also activate glia, inducing pro-inflammatory cytokine and chemokine production, which counter-regulates the analgesic properties of classical opioid receptor activation. It is not known how long these adverse pro-inflammatory effects last or whether prior morphine could sensitize the central nervous system (CNS) such that responses to a subsequent injury/inflammation would be exacerbated. Here, multiple models of inflammation or injury were induced two days after morphine (5mg/kg b.i.d., five days , s.c.) to test the generality of morphine sensitization of later pain. Prior repeated morphine potentiated the duration of allodynia from peripheral inflammatory challenges (complete Freund's adjuvant (CFA) into either hind paw skin or masseter muscle) and from peripheral neuropathy (mild chronic constriction injury (CCI) of the sciatic nerve). Spinal cord and trigeminal nucleus caudalis mRNAs were analyzed to identify whether repeated morphine was sufficient to alter CNS expression of pro-inflammatory response genes, measured two days after cessation of treatment. Prior morphine elevated IL-1ß mRNA at both sites, MHC-II and TLR4 in the trigeminal nucleus caudalis but not spinal cord, but not glial activation markers at either site. Finally, in order to identify whether morphine sensitized pro-inflammatory cytokine release, spinal cord was isolated two days after morphine dosing for five days , and slices stimulated ex vivo with lipopolysaccharide. The morphine significantly induced TNFα protein release. Therefore, repeated morphine is able to sensitize subsequent CNS responses to immune challenges.

Evidence for a navigational map stretching across the continental U.S. in a migratory songbird.

Billions of songbirds migrate several thousand kilometers from breeding to wintering grounds and are challenged with crossing ecological barriers and facing displacement by winds along the route. A satisfactory explanation of long-distance animal navigation is still lacking, partly because of limitations on field-based study. The navigational tasks faced by adults and juveniles differ fundamentally, because only adults migrate toward wintering grounds known from the previous year. Here, we show by radio tracking from small aircraft that only adult, and not juvenile, long-distance migrating white-crowned sparrows rapidly recognize and correct for a continent-wide displacement of 3,700 km from the west coast of North America to previously unvisited areas on the east coast. These results show that the learned navigational map used by adult long-distance migratory songbirds extends at least on a continental scale. The juveniles with less experience rely on their innate program to find their distant wintering areas and continue to migrate in the innate direction without correcting for displacement.

Comparing aerodynamic efficiency in birds and bats suggests better flight performance in birds.

Flight is one of the energetically most costly activities in the animal kingdom, suggesting that natural selection should work to optimize flight performance. The similar size and flight speed of birds and bats may therefore suggest convergent aerodynamic performance; alternatively, flight performance could be restricted by phylogenetic constraints. We test which of these scenarios fit to two measures of aerodynamic flight efficiency in two passerine bird species and two New World leaf-nosed bat species. Using time-resolved particle image velocimetry measurements of the wake of the animals flying in a wind tunnel, we derived the span efficiency, a metric for the efficiency of generating lift, and the lift-to-drag ratio, a metric for mechanical energetic flight efficiency. We show that the birds significantly outperform the bats in both metrics, which we ascribe to variation in aerodynamic function of body and wing upstroke: Bird bodies generated relatively more lift than bat bodies, resulting in a more uniform spanwise lift distribution and higher span efficiency. A likely explanation would be that the bat ears and nose leaf, associated with echolocation, disturb the flow over the body. During the upstroke, the birds retract their wings to make them aerodynamically inactive, while the membranous bat wings generate thrust and negative lift. Despite the differences in performance, the wake morphology of both birds and bats resemble the optimal wake for their respective lift-to-drag ratio regimes. This suggests that evolution has optimized performance relative to the respective conditions of birds and bats, but that maximum performance is possibly limited by phylogenetic constraints. Although ecological differences between birds and bats are subjected to many conspiring variables, the different aerodynamic flight efficiency for the bird and bat species studied here may help explain why birds typically fly faster, migrate more frequently and migrate longer distances than bats.

Vortex wake, downwash distribution, aerodynamic performance and wingbeat kinematics in slow-flying pied flycatchers.

Many small passerines regularly fly slowly when catching prey, flying in cluttered environments or landing on a perch or nest. While flying slowly, passerines generate most of the flight forces during the downstroke, and have a 'feathered upstroke' during which they make their wing inactive by retracting it close to the body and by spreading the primary wing feathers. How this flight mode relates aerodynamically to the cruising flight and so-called 'normal hovering' as used in hummingbirds is not yet known. Here, we present time-resolved fluid dynamics data in combination with wingbeat kinematics data for three pied flycatchers flying across a range of speeds from near hovering to their calculated minimum power speed. Flycatchers are adapted to low speed flight, which they habitually use when catching insects on the wing. From the wake dynamics data, we constructed average wingbeat wakes and determined the time-resolved flight forces, the time-resolved downwash distributions and the resulting lift-to-drag ratios, span efficiencies and flap efficiencies. During the downstroke, slow-flying flycatchers generate a single-vortex loop wake, which is much more similar to that generated by birds at cruising flight speeds than it is to the double loop vortex wake in hovering hummingbirds. This wake structure results in a relatively high downwash behind the body, which can be explained by the relatively active tail in flycatchers. As a result of this, slow-flying flycatchers have a span efficiency which is similar to that of the birds in cruising flight and which can be assumed to be higher than in hovering hummingbirds. During the upstroke, the wings of slowly flying flycatchers generated no significant forces, but the body-tail configuration added 23 per cent to weight support. This is strikingly similar to the 25 per cent weight support generated by the wing upstroke in hovering hummingbirds. Thus, for slow-flying passerines, the upstroke cannot be regarded as inactive, and the tail may be of importance for flight efficiency and possibly manoeuvrability.

The role of wind-tunnel studies in integrative research on migration biology.

Wind tunnels allow researchers to investigate animals' flight under controlled conditions, and provide easy access to the animals during flight. These increasingly popular devices can benefit integrative migration biology by allowing us to explore the links between aerodynamic theory and migration as well as the links between flight behavior and physiology. Currently, wind tunnels are being used to investigate many different migratory phenomena, including the relationship between metabolic power and flight speed and carry-over effects between different seasons. Although biotelemetry is also becoming increasingly common, it is unlikely that it will be able to completely supplant wind tunnels because of the difficulty of measuring or varying parameters such as flight speed or temperature in the wild. Wind tunnels and swim tunnels will therefore continue to be important tools we can use for studying integrative migration biology.

Grand challenges in migration biology.

Billions of animals migrate each year. To successfully reach their destination, migrants must have evolved an appropriate genetic program and suitable developmental, morphological, physiological, biomechanical, behavioral, and life-history traits. Moreover, they must interact successfully with biotic and abiotic factors in their environment. Migration therefore provides an excellent model system in which to address several of the "grand challenges" in organismal biology. Previous research on migration, however, has often focused on a single aspect of the phenomenon, largely due to methodological, geographical, or financial constraints. Integrative migration biology asks 'big questions' such as how, when, where, and why animals migrate, which can be answered by examining the process from multiple ecological and evolutionary perspectives, incorporating multifaceted knowledge from various other scientific disciplines, and using new technologies and modeling approaches, all within the context of an annual cycle. Adopting an integrative research strategy will provide a better understanding of the interactions between biological levels of organization, of what role migrants play in disease transmission, and of how to conserve migrants and the habitats upon which they depend.

Pointed wings, low wingloading and calm air reduce migratory flight costs in songbirds.

Migratory bird, bat and insect species tend to have more pointed wings than non-migrants. Pointed wings and low wingloading, or body mass divided by wing area, are thought to reduce energy consumption during long-distance flight, but these hypotheses have never been directly tested. Furthermore, it is not clear how the atmospheric conditions migrants encounter while aloft affect their energy use; without such information, we cannot accurately predict migratory species' response(s) to climate change. Here, we measured the heart rates of 15 free-flying Swainson's Thrushes (Catharus ustulatus) during migratory flight. Heart rate, and therefore rate of energy expenditure, was positively associated with individual variation in wingtip roundedness and wingloading throughout the flights. During the cruise phase of the flights, heart rate was also positively associated with wind speed but not wind direction, and negatively but not significantly associated with large-scale atmospheric stability. High winds and low atmospheric stability are both indicative of the presence of turbulent eddies, suggesting that birds may be using more energy when atmospheric turbulence is high. We therefore suggest that pointed wingtips, low wingloading and avoidance of high winds and turbulence reduce flight costs for small birds during migration, and that climate change may have the strongest effects on migrants' in-flight energy use if it affects the frequency and/or severity of high winds and atmospheric instability.

Wingbeat frequency and flap-pause ratio during natural migratory flight in thrushes.

Powered flapping flight has evolved independently in many different taxa. For flapping fliers, wingbeat parameters such as frequency and amplitude are the primary determinants of these animals' energetic expenditure during flight. Here we present data on wingbeat frequency and amplitude for three New World thrush species during 15 entire nocturnal migratory flights over the Midwestern United States. Using continuous (non-pulsing) radio transmitters, we were able to measure wingbeat frequency and relative amplitude of wingbeats as well as the characteristics of flap-pauses. Contrary to previous telemetric findings, all of the individuals we followed used both flapping-only and flap-pause flight. During migratory flights, wingbeat frequency, effective wingbeat frequency, and amplitude were highest during initial ascent. Effective wingbeat frequency and amplitude were lowest during final descent. We show that identification of species based solely on characteristics of the wingbeat e.g., during radar studies, can be difficult because variables such as wingbeat frequency and amplitude, wingbeat pausing, and pattern of beats and pauses vary between individuals of the same species and even within individual flights. We also show that observed wingbeat frequencies were lower than those predicted by theoretical models. We speculate that this may be because theoretical predictions are generally based on (1) data from larger birds and (2) data from diurnal flights. We found that diurnal wingbeat frequencies of thrushes were generally higher than were those during nocturnal migratory flight. Finally, we suggest that rather than remaining at a single altitude during flight or climbing slightly as theoretical models predict, thrushes often moved up and down in the air column, perhaps searching for favorable atmospheric conditions.

Biotelemetry of New World thrushes during migration: Physiology, energetics and orientation in the wild.

Billions of songbirds migrate between continents each year, but we have yet to obtain enough information on in-flight physiology and energetics to fully understand the migratory behavior of any one species. New World Catharus thrushes are common nocturnal migrants amenable to biotelemetry, allowing us to measure physiological parameters during migratory flight in the wild. Here, we review work by the authors on Catharus thrush in-flight physiology during spring migration in continental North America and present new data on individual variation in energy use during migratory flight. Previous work demonstrated that (1) a number of simple behavioral rules are sufficient to explain the initiation of individual migratory flights made by Catharus thrushes, (2) the thrushes used a magnetic compass to orient during the night rather than celestial cues and that they calibrated this magnetic compass each day using cues associated with the setting sun, (3) in total, Catharus thrushes used approximately twice as much energy during stopovers than they used during migratory flight, and (4) thrushes may use more energy when thermoregulating on cold days than on days when they make short migratory flights. Recently, we built upon this work and used newly-developed transmitters to measure heart rate, wingbeat frequency and respiration rate of free-flying Swainson's Thrushes (C. ustulatus). We found a large amount of between-individual variation in average heart rate after ascent (range 12.06-14.81 Hz, mean ± SD, 13.48 ± 0.75, n = 10), average wingbeat frequency after ascent (10.25-11.75 Hz, 10.82 ± 0.49, n = 10), and the difference between the two variables (1.5-3.84 Hz, 2.53 ± 0.76, n = 8). Both heart rate and wingbeat frequency were significantly higher during ascent than later in the flight. We propose biotelemetry as a means to understand energetic trade-offs and decisions during natural migratory flight in songbirds. To further our knowledge of intercontinental songbird migration and the connectivity between wintering and breeding sites, we outline plans for a satellite-based global tracking system for <1 g transmitters.