Pervasive mimicry in flight behavior among aposematic butterflies.

Flight was a key innovation in the adaptive radiation of insects. However, it is a complex trait influenced by a large number of interacting biotic and abiotic factors, making it difficult to unravel the evolutionary drivers. We investigate flight patterns in neotropical heliconiine butterflies, well known for mimicry of their aposematic wing color patterns. We quantify the flight patterns (wing beat frequency and wing angles) of 351 individuals representing 29 heliconiine and 9 ithomiine species belonging to ten color pattern mimicry groupings. For wing beat frequency and up wing angles, we show that heliconiine species group by color pattern mimicry affiliation. Convergence of down wing angles to mimicry groupings is less pronounced, indicating that distinct components of flight are under different selection pressures and constraints. The flight characteristics of the Tiger mimicry group are particularly divergent due to convergence with distantly related ithomiine species. Predator-driven selection for mimicry also explained variation in flight among subspecies, indicating that this convergence can occur over relatively short evolutionary timescales. Our results suggest that the flight convergence is driven by aposematic signaling rather than shared habitat between comimics. We demonstrate that behavioral mimicry can occur between lineages that have separated over evolutionary timescales ranging from <0.5 to 70 My.

Temperature effects on Mormon cricket Anabrus simplex embryo development, hatching and nymphal growth: Thermal performance curves change with ontogeny.

Thermal performance curves for development are an essential tool for population modeling and pest management. More broadly, they characterize how selection on thermal limits or maximum rates change with life stage. The effects of temperature on development of Mormon cricket embryos, and hatching and development of nymphs were measured on a population from the Bighorn Mountains of Wyoming and modeled with four non-linear equations. Taylor's Gaussian curve characterized embryonic development, which was most rapid at 26.9 °C. However, half-grown embryos aestivated at high temperatures, resulting in a significant shift in the optimum temperature to complete embryonic development to 24.1 °C and a reduction in the breadth of the performance curve (thermal breadth). Fully grown embryos hatched fastest at relatively low temperatures (21.8 °C), whereas nymphal development was maximized at relatively high temperatures (35.7 °C). Thermal breadths for nymphal hatching and development were also significantly broader than that for embryonic development. Differences in optimum temperature and thermal breadth of each life stage should be taken into consideration in population modeling, comparisons among populations, and epigenetic studies of acclimation.

Prolonged diapause in Mormon crickets: Embryonic responses to three measures of time.

Mormon cricket eggs can remain diapausing in soil for multiple years without forming an embryo. I investigated whether embryonic development was dependent on the number of annual cycles since the egg was laid, duration of the summer period (forcing), or duration of the winter period (chilling). Male and female Mormon crickets collected in Arizona and Wyoming were paired in the lab. For each mating pair, sibling eggs were incubated 12 weeks, eggs with fully developed embryos removed, and the remaining eggs were split evenly among three treatments: a long cold period and a long warm period; a short cold period and a long warm period; and a short cold period and a short warm period, which respectively completed 2 annual cycles, 3 cycles, and 4 cycles in 60 calendar weeks. In each cycle over nine years, developed eggs and eggs that appeared inviable were counted and removed. For each mating pair, I used survival analyses to test for differences in 1) the number of annual cycles, 2) the warm period duration, and 3) the cold period duration required for the embryos to develop. For eight of 11 mating pairs, one of the three factors was not excluded as a determinant of the phenology of embryonic development. Duration of the warm period was not rejected in seven of 11 cases. Duration of the warm period required for 50 % of the eggs to develop ranged from 84 to 144 weeks. In one case from Arizona, the duration of the cold period was the only factor not rejected. Median chill time was 60 weeks, which is also more than one year. Despite this exception, I conclude that duration of the warm period is typically the factor that determines timing of embryonic development for Mormon crickets. For these two high elevation populations, median forcing or chilling exceeded one year.

Effects of parental diet on Mormon cricket egg diapause, embryonic development rate, and periodic outbreaks.

Transgenerational phenotypic modification can alter organismal fitness, population demographics, and community interactions. For ectotherms, both dietary composition and temperature have important effects on organismal fitness, but they are rarely investigated together. Mormon crickets Anabrus simplex are capable of diapausing as eggs in the soil for multiple years with duration largely dependent on cumulative heat units or degree days. Because Mormon crickets can be abundant in the landscape in one year and disappear suddenly the next, I asked: does parental nutrition affect the duration of egg diapause? Beginning in the ultimate nymphal instar, Mormon crickets were fed a diet high in protein, one equal in protein to carbohydrate, or a diet high in carbohydrates and the time for eggs to develop after they were laid was measured. If parental nutrition affects temperature-sensitive egg diapause, then that change in sensitivity to temperature might also alter the relationship between embryonic development rate and temperature. I asked: does parental nutrition affect embryonic development rate as a function of temperature? To this end, I manipulated densities of Mormon cricket nymphs and protein-rich prey (grasshoppers) in field cages, collected eggs from the adult Mormon crickets, and measured the optimal temperature, maximum development rate, and thermal breadth for embryonic development of the offspring. I found that Mormon crickets fed a high protein diet laid eggs with shorter diapause. Consistent with this long-term result, those housed with the most grasshoppers to eat laid eggs that had the fastest maximum development rate, whereas those without grasshoppers laid eggs with slower maximum developmental rates but the broadest thermal breadth. Eggs from Mormon crickets housed with intermediate levels of grasshopper densities had a decline in peak development rate with an increase in density. In addition, Mormon crickets housed with more conspecifics laid eggs with faster development rates, whereas thermal breadth and the temperature optima were not affected by cricket density. As predicted, Mormon cricket diets significantly affected egg diapause and development rates. Contrary to expectations based on observed changes in diet preferences during a Mormon cricket outbreak, Mormon crickets fed high protein diets laid eggs with significantly shorter egg diapause and significantly faster egg development rates. Interestingly, doubling of Mormon cricket density caused eggs to develop in nearly half the time. This latter result indicates that Mormon cricket aggregations promote rapid development of progeny. Moreover, the tight, linear structure of migratory bands in which females intermittently stop to lay eggs assures that the progeny hatch and develop in dense cohorts. In this manner, the banding behavior might carry-over into subsequent generations as long as cohorts are dense and protein is available. With band thinning or protein restriction, females spread their bet-hedging and progeny remain longer as eggs in the soil.

Selective protein self-deprivation by Mormon crickets following fungal attack.

Immune responses to infection result in behavioral changes that affect resource acquisition, such as general starvation and compensatory feeding to offset changes in resource allocation. Mormon crickets aggregate and march in bands containing millions of insects. Some bands are comprised of insects seeking proteins. They are also low in circulating phenoloxidase (PO) and more susceptible to fungal attack, as we have demonstrated in the lab. Here, we ask: Do Mormon crickets elevate PO and consume protein in response to infection by the pathogenic fungus Beauveria bassiana? B. bassiana was applied topically (day 0), and mortality began on day 5. Total protein, PO, and prophenoloxidase (proPO) were assayed in hemolymph on day 1 and 4. On day 1, PO titers were not different between inoculated and control insects, whereas by day 4, PO was greater in the inoculated group. proPO activity was unchanged. Circulating protein declined in inoculated insects relative to controls. As predicted, PO titers were elevated as a result of fungal infection, and hemolymph protein was reduced, but the insects did not compensate behaviorally. Indeed, during the first three days post-infection, infected insects reduced protein consumption while maintaining carbohydrate consumption similar to the controls. Following day 3, a more general reduction in protein and carbohydrate intake was evident in infected insects. Survivorship to infection was associated with the amount of protein consumed and unrelated to carbohydrate consumption. Selective protein deprivation by the host seems counterintuitive, but it might limit growth and toxin production by the invading fungus. Alternatively, the fungus might control the host diet to compromise host immunity to infection. Abrupt changes in allocation resulting from an infection can lead to changes in acquisition that are not always intuitive. Because protein acquisition drives aggression between members of the migratory band, B. bassiana application may reduce cannibalism and slow band movement.

Power Bars: Mormon Crickets Get Immunity Boost from Eating Grasshoppers.

In addition to feeding on plants, Mormon crickets Anabrus simplex Haldeman, 1852 predate on invertebrates, including one another, which effectively drives their migration. Carnivory derives from lack of dietary protein, with Mormon crickets deprived of protein having less phenoloxidase (PO) available to combat foreign invaders, such as fungal pathogens. Because Mormon crickets commonly occur with grasshoppers that feed on the same plants, we investigated interactions between grasshoppers and Mormon crickets, and hypothesized that if Mormon crickets are predatory on grasshoppers, grasshopper abundance would influence the protein available to Mormon crickets and their immunity. In a field setting, we varied densities of Mormon crickets (0, 10, or 20 per cage) and grasshoppers Melanoplus borealis (0, 15, 30, or 45) in 68 1-m2 cages. After one month, we measured Mormon cricket dietary preferences and PO activity. As predicted, artificial diet consumption shifted away from protein as grasshopper density increased, and immunocompetence, as measured by PO activity, also increased with grasshopper availability. Although nitrogen availability in the vegetation decreased with increasing insect density, predation became an important source of protein for Mormon crickets that enhanced immunity. Grasshoppers can be an important source of dietary protein for Mormon crickets, with prey availability affecting Mormon cricket immunity to diseases.

Quantifying the Aerodynamic Power Required for Flight and Testing for Adaptive Wind Drift in Passion-Vine Butterflies Heliconius sara (Lepidoptera: Nymphalidae).

Although theoretical work on optimal migration has been largely restricted to birds, relevant free-flight data are now becoming available for migratory insects. Here we report, for the first time in passion-vine butterflies, that Heliconius sara migrates directionally. To test optimal migration models for insects, we quantified the aerodynamic power curve for free-flying H. sara as they migrated across the Panama Canal. Using synchronized stereo-images from high-speed video cameras, we reconstructed three-dimensional flight kinematics of H. sara migrating naturally across the Panama Canal. We also reconstructed flight kinematics from a single-camera view of butterflies flying through a flight tunnel. We calculated the power requirements for flight for H. sara over a range of flight velocities. The relationship between aerodynamic power and velocity was "J"-shaped across the measured velocities with a minimum power velocity of 0.9 m/s and a maximum range velocity of 2.25 m/s. Migrating H. sara did not compensate for crosswind drift. Changes in airspeed with tailwind drift were consistent with the null hypothesis that H. sara did not compensate for tailwind drift, but they were also not significantly different from those predicted to maximize the migratory range of the insects.

Elevational Changes in Mormon Cricket Life Histories: Minimum Temperature for Nymphal Growth Declines With Elevation.

As the mean temperature and the duration of the growing season decline with elevation, growth of immature insects should initiate at a lower temperature, but it should also be faster to complete development prior to season's end. Although flightless, Mormon crickets migrate in large aggregations across broad spatial and elevational distances that might limit adaptations to local environments. In addition, selection to be active at cooler temperatures might limit selection to maximize growth rate. I measured growth rate in controlled environments for nymphs from three populations that vary in altitude (87-2,688 m) but are similar in latitude (43.2-45.7°N). Growth rate increased significantly with mean rearing temperature between 22 and 30°C. The intercept of the regression of growth rate on temperature increased with elevation, whereas the slope did not change significantly. For any given rearing temperature, growth rate increased with elevation, which suggests that selection to initiate growth at cooler temperatures did not compromise growth rate. Body mass did not differ between the two lower elevations, whereas the highest elevation population had smaller hatchlings and adults. Critical thermal minimum (base temperature) declined with elevation (0.7°C per 1,000 m), and the degree days were 509 across all elevations. For pest management, a base temperature from midelevation of 15.3°C (60°F) and growing degree days of 509 (equivalent to 916 Fahrenheit-based degree days) are reasonable estimates for applications from sea level to 2,700 m.

Elevational and Latitudinal Changes in Cold Tolerance of Nymph and Adult Mormon Crickets Anabrus simplex (Orthoptera: Tettigoniidae).

Insects that hatch in winter and early spring in desert and montane regions are likely to encounter extreme weather events, including precipitous drops in temperature. The susceptibility of insects to exposure to subzero temperatures is predicted to decrease with increasing latitude or elevation. Mormon crickets occur over a broad latitudinal range from southwestern United States to Canada and a broad elevational range from near sea-level to 3,000 m. Population declines have been attributed to late freezing events, but winter hatching suggests they may also be cold tolerant. Lower lethal temperature of high elevation populations in low latitude Arizona (AZ) and high latitude Wyoming (WY) was measured by exposing nymphs and adults to 6 h or 24 h of subzero temperature. From similar latitude, WY was compared with mid-elevation Idaho (ID) and low elevation Oregon (OR) populations. Contrary to the prediction, lethal temperature of third instar nymphs was lower in AZ than in the more northerly populations. Consistently, AZ was more tolerant of cold in early nymphal instars relative to populations from higher latitude. Early hatching at lower latitudes might increase the risk of early instars experiencing a severe cold snap relative to nymphs at high latitudes. Also, contrary to prediction, the lethal temperature of adults increased with elevation, whereas third instar nymphs from mid-elevation ID were the most susceptible to cold exposure. Cold tolerance in immature and mature stages is more likely to be uncoupled when life stages do not coincide, as with Mormon crickets.

Predation landscapes influence migratory prey ecology and evolution.

Migratory prey experience spatially variable predation across their life cycle. They face unique challenges in navigating this predation landscape, which affects their perception of risk, antipredator responses, and resulting mortality. Variable and unfamiliar predator cues during migration can limit accurate perception of risk and migrants often rely on social information and learning to compensate. The energetic demands of migration constrain antipredator responses, often through context-dependent patterns. While migration can increase mortality, migrants employ diverse strategies to balance risks and rewards, including life history and antipredator responses. Humans interact frequently with migratory prey across space and alter both mortality risk and antipredator responses, which can scale up to affect migratory populations and should be considered in conservation and management.

Antennal regulation of migratory flight in the neotropical moth Urania fulgens.

Migrating insects use their sensory systems to acquire local and global cues about their surroundings. Previous research on tethered insects suggests that, in addition to vision and cephalic bristles, insects use antennal mechanosensory feedback to maintain their airspeeds. Owing to the large displacements of migratory insects and difficulties inherent in tracking single individuals, the roles of these sensory inputs have never been tested in freely migrating insects. We tracked individual uraniid moths (Urania fulgens) as they migrated diurnally over the Panama Canal, and measured airspeeds and orientation for individuals with either intact or amputated flagella. Consistent with prior observations that antennal input is necessary for flight control, 59 per cent of the experimental moths could not fly after flagella amputation. The remaining fraction (41%) was flight-capable and maintained its prior airspeeds despite severe reduction in antennal input. Thus, maintenance of airspeeds may not involve antennal input alone, and is probably mediated by other modalities. Moths with amputated flagella could not recover their proper migratory orientations, suggesting that antennal integrity is necessary for long-distance navigation.

Parental Photoperiod Affects Egg Diapause in a Montane Population of Mormon Crickets (Orthoptera: Tettigoniidae).

Insect diapause is a state of arrested development persisting when conditions are favorable for growth. Prolonged diapause, which occurs when insects remain in diapause for multiple years, is uncommon. Mormon crickets Anabrus simplex Haldane, a katydid and pest of rangeland forage and crops, were thought to be biennial in the Bighorn Mountains of Wyoming, but they are able to prolong diapause in the egg stage for multiple years. To test whether parental photoperiod serves as a cue to prolong diapause, mating pairs from the Bighorn Mountains were set in the same daily temperature and humidity profiles with 20 pairs on short daylength (12:12 [L:D] h) and 20 on long daylength (15:9 [L:D] h). Almost every parental pair had some undeveloped eggs after two warm periods. Females in short daylength were not more likely to have eggs with a biennial life cycle, but they were more likely than those in long daylength to lay eggs with multi-annual life cycles. Parents on short daylength were more likely to lay inviable eggs. Other fitness measures, such as hatchling mass, nymphal survivorship, and adult mass were not different between parental treatments. Diapause termination distributed over multiple years probably constitutes a bet-hedging strategy in an unpredictable environment.

Experimental Manipulation of Dispersal Ability in A Neotropical Butterfly Anartia fatima (Lepidoptera: Nymphalidae).

Research on endangered British butterflies has found that butterfly populations in small refuges evolve to allocate more mass to the thorax (flight muscle) and less to the abdomen than populations in large refuges. The observed change in mass allocation affects two morphological features relevant to flight: the flight muscle ratio (FMR) and the position of center of body mass (cmbody). The author tested whether a decrease in FMR or a change in cmbody reduced the ability to disperse by experimentally weight-loading Neotropical Anartia fatima butterflies. In one treatment group, FMR was decreased but cmbody was not altered, whereas in the second group FMR was decreased and cmbody was repositioned further posterior. In one mark⁻release⁻recapture (MRR) experiment, butterflies dispersed relatively slowly, and treatment groups did not differ significantly. In a replicate experiment, butterflies dispersed more quickly, and control butterflies dispersed more rapidly than either treatment group. Differences in dispersal were consistent with a causal relationship between FMR and movement. A more posterior cmbody had little effect on dispersal beyond that due to the change in FMR. These results support the hypothesis that an increase in mass allocation to the thorax in small, dispersed refugia is due to selection on the ability to disperse.

A Laboratory Curse: Variation in Temperature Stimulates Embryonic Development and Shortens Diapause.

An ongoing biological debate concerns the difference in trait expression in continuous versus cycling temperature regimes, but are even daily cycling temperatures sufficient to generate natural expression of traits? We compared embryonic development and the duration of diapause for Mormon cricket Anabrus simplex Haldeman (Orthoptera: Tettigoniidae) eggs incubated in a daily cycling temperature constant in both amplitude and thermoperiod with those in a cycling temperature that was patterned after natural fluctuations in ambient temperature. Although the proportion of eggs developing did not differ between treatments, 128 d of vernalization was required to hatch after incubation in the constant cycling treatment relative to 42 d in the more variable cycle. We then compared these same development and diapause traits for eggs incubated in a daily cycling temperature that was constant in amplitude but varied in thermoperiod with those in the cycling temperature patterned after natural fluctuations in ambient temperature. The proportion of eggs developing in this constant cycling treatment was nearly half that in the variable treatment, and 128 d was insufficient time to break diapause following the constant cycling treatment even though the thermoperiods were now more similar. We have found that variation in the cycling temperature to mimic natural fluctuations in amplitude and period broadens the time when eggs can be warmed up for hatching and improves hatching success. Daily cycling temperatures that are constant over the season are insufficient to generate natural trait expression.

Evolution of the wave: aerodynamic and aposematic functions of butterfly wing motion.

Many unpalatable butterfly species use coloration to signal their distastefulness to birds, but motion cues may also be crucial to ward off predatory attacks. In previous research, captive passion-vine butterflies Heliconius mimetic in colour pattern were also mimetic in motion. Here, I investigate whether wing motion changes with the flight demands of different behaviours. If birds select for wing motion as a warning signal, aposematic butterflies should maintain wing motion independently of behavioural context. Members of one mimicry group (Heliconius cydno and Heliconius sapho) beat their wings more slowly and their wing strokes were more asymmetric than their sister-species (Heliconius melpomene and Heliconius erato, respectively), which were members of another mimicry group having a quick and steady wing motion. Within mimicry groups, wing beat frequency declined as its role in generating lift also declined in different behavioural contexts. In contrast, asymmetry of the stroke was not associated with wing beat frequency or behavioural context-strong indication that birds process and store the Fourier motion energy of butterfly wings. Although direct evidence that birds respond to subtle differences in butterfly wing motion is lacking, birds appear to generalize a motion pattern as much as they encounter members of a mimicry group in different behavioural contexts.

Partitioning the effects of mating and nuptial feeding on the microbiome in gift-giving insects.

Mating is a ubiquitous social interaction with the potential to influence the microbiome by facilitating transmission, modifying host physiology, and in species where males donate nuptial gifts to females, altering diet. We manipulated mating and nuptial gift consumption in two insects that differ in nuptial gift size, the Mormon cricket Anabrus simplex and the decorated cricket Gryllodes sigillatus, with the expectation that larger gifts are more likely to affect the gut microbiome. Surprisingly, mating, but not nuptial gift consumption, affected the structure of bacterial communities in the gut, and only in Mormon crickets. The change in structure was due to a precipitous drop in the abundance of lactic-acid bacteria in unmated females, a taxon known for their beneficial effects on nutrition and immunity. Mating did not affect phenoloxidase or lysozyme-like antibacterial activity in either species, suggesting that any physiological response to mating on host-microbe interactions is decoupled from systemic immunity. Protein supplementation also did not affect the gut microbiome in decorated crickets, suggesting that insensitivity of gut microbes to dietary protein could contribute to the lack of an effect of nuptial gift consumption. Our study provides experimental evidence that sexual interactions can affect the microbiome and suggests mating can promote beneficial gut bacteria.

Spatial Structure of the Mormon Cricket Gut Microbiome and its Predicted Contribution to Nutrition and Immune Function.

The gut microbiome of insects plays an important role in their ecology and evolution, participating in nutrient acquisition, immunity, and behavior. Microbial community structure within the gut is heavily influenced by differences among gut regions in morphology and physiology, which determine the niches available for microbes to colonize. We present a high-resolution analysis of the structure of the gut microbiome in the Mormon cricket Anabrus simplex, an insect known for its periodic outbreaks in the western United States and nutrition-dependent mating system. The Mormon cricket microbiome was dominated by 11 taxa from the Lactobacillaceae, Enterobacteriaceae, and Streptococcaceae. While most of these were represented in all gut regions, there were marked differences in their relative abundance, with lactic-acid bacteria (Lactobacillaceae) more common in the foregut and midgut and enteric (Enterobacteriaceae) bacteria more common in the hindgut. Differences in community structure were driven by variation in the relative prevalence of three groups: a Lactobacillus in the foregut, Pediococcus lactic-acid bacteria in the midgut, and Pantoea agglomerans, an enteric bacterium, in the hindgut. These taxa have been shown to have beneficial effects on their hosts in insects and other animals by improving nutrition, increasing resistance to pathogens, and modulating social behavior. Using PICRUSt to predict gene content from our 16S rRNA sequences, we found enzymes that participate in carbohydrate metabolism and pathogen defense in other orthopterans. These were predominately represented in the hindgut and midgut, the most important sites for nutrition and pathogen defense. Phylogenetic analysis of 16S rRNA sequences from cultured isolates indicated low levels of divergence from sequences derived from plants and other insects, suggesting that these bacteria are likely to be exchanged between Mormon crickets and the environment. Our study shows strong spatial variation in microbiome community structure, which influences predicted gene content and thus the potential of the microbiome to influence host function.

Loss of safety in numbers and a novel driver of mass migration: radiotelemetry reveals heavy wasp predation on a band of Mormon crickets.

Coordinated movement of animals is a spectacular phenomenon that has received much attention. Experimental studies of Mormon crickets and locust nymphs have demonstrated that collective motion can arise from cannibalism that compensates for nutritional deficiencies arising from group living. Grouping into migratory bands confers protection from predators. By radiotracking migrating, Mormon crickets released over 3 days, we found that specialized, parasitoid digger wasps (Sphecidae) respond numerically and prey heavily on aggregated Mormon crickets leading to loss of safety in numbers. Palmodes laeviventris paralysed and buried 42% of tagged females and 8% of the males on the final day of tracking. Risk of wasps and Mormon crickets hatching on the same site is high and may drive nymphal emigration. A preference to provision offspring with adult female Mormon crickets can be explained by their greater fat content and larger size compared with males, improving survival of wasps during diapause.

The Butterflies of Barro Colorado Island, Panama: Local Extinction since the 1930s.

Few data are available about the regional or local extinction of tropical butterfly species. When confirmed, local extinction was often due to the loss of host-plant species. We used published lists and recent monitoring programs to evaluate changes in butterfly composition on Barro Colorado Island (BCI, Panama) between an old (1923-1943) and a recent (1993-2013) period. Although 601 butterfly species have been recorded from BCI during the 1923-2013 period, we estimate that 390 species are currently breeding on the island, including 34 cryptic species, currently only known by their DNA Barcode Index Number. Twenty-three butterfly species that were considered abundant during the old period could not be collected during the recent period, despite a much higher sampling effort in recent times. We consider these species locally extinct from BCI and they conservatively represent 6% of the estimated local pool of resident species. Extinct species represent distant phylogenetic branches and several families. The butterfly traits most likely to influence the probability of extinction were host growth form, wing size and host specificity, independently of the phylogenetic relationships among butterfly species. On BCI, most likely candidates for extinction were small hesperiids feeding on herbs (35% of extinct species). However, contrary to our working hypothesis, extinction of these species on BCI cannot be attributed to loss of host plants. In most cases these host plants remain extant, but they probably subsist at lower or more fragmented densities. Coupled with low dispersal power, this reduced availability of host plants has probably caused the local extinction of some butterfly species. Many more bird than butterfly species have been lost from BCI recently, confirming that small preserves may be far more effective at conserving invertebrates than vertebrates and, therefore, should not necessarily be neglected from a conservation viewpoint.

The aerodynamic costs of warning signals in palatable mimetic butterflies and their distasteful models.

Bates hypothesized that some butterfly species that are palatable gain protection from predation by appearing similar to distasteful butterflies. When undisturbed, distasteful butterflies fly slowly and in a straight line, and palatable Batesian mimics also adopt this nonchalant behaviour. When seized by predators, distasteful butterflies are defended by toxic or nauseous chemicals. Lacking chemical defences, Batesian mimics depend on flight to escape attacks. Here, I demonstrate that flight in warning-coloured mimetic butterflies and their distasteful models is more costly than in closely related non-mimetic butterflies. The increased cost is the result of differences in both wing shape and kinematics. Batesian mimics and their models slow the angular velocity of their wings to enhance the colour signal but at an aerodynamic cost. Moreover, the design for flight in Batesian mimics has an additional energetic cost over that of its models. The added cost may cause Batesian mimics to be rare, explaining a general pattern that Bates first observed.