Modeling scale up of anthropogenic impacts from individual pollinator behavior to pollination systems.

Understanding how anthropogenic disturbances affect plant-pollinator systems has important implications for the conservation of biodiversity and ecosystem functioning. Previous laboratory studies show that pesticides and pathogens, which have been implicated in the rapid global decline of pollinators over recent years, can impair behavioral processes needed for pollinators to adaptively exploit floral resources and effectively transfer pollen among plants. However, the potential for these sublethal stressor effects on pollinator-plant interactions at the individual level to scale up into changes to the dynamics of wild plant and pollinator populations at the system level remains unclear. We developed an empirically parameterized agent-based model of a bumblebee pollination system called SimBee to test for effects of stressor-induced decreases in the memory capacity and information processing speed of individual foragers on bee abundance (scenario 1), plant diversity (scenario 2), and bee-plant system stability (scenario 3) over 20 virtual seasons. Modeling of a simple pollination network of a bumblebee and four co-flowering bee-pollinated plant species indicated that bee decline and plant species extinction events could occur when only 25% of the forager population showed cognitive impairment. Higher percentages of impairment caused 50% bee loss in just five virtual seasons and system-wide extinction events in less than 20 virtual seasons under some conditions. Plant species extinctions occurred regardless of bee population size, indicating that stressor-induced changes to pollinator behavior alone could drive species loss from plant communities. These findings indicate that sublethal stressor effects on pollinator behavioral mechanisms, although seemingly insignificant at the level of individuals, have the cumulative potential in principle to degrade plant-pollinator species interactions at the system level. Our work highlights the importance of an agent-based modeling approach for the identification and mitigation of anthropogenic impacts on plant-pollinator systems.

Aumento en el Modelado de los Impactos Antropogénicos de Polinizador Individual a Sistemas de Polinización Resumen El entendimiento de cómo las perturbaciones antropogénicas afectan a los sistemas planta-polinizador tiene consecuencias importantes para la conservación de la biodiversidad y el funcionamiento del ecosistema. Los estudios previos realizados en laboratorios muestran que los pesticidas y los patógenos, los cuales han estado implicados en la rápida declinación global de los polinizadores en los años recientes, pueden perjudicar los procesos de comportamiento necesarios para que los polinizadores exploten adaptativamente los recursos florales y transfieran de manera efectiva el polen entre las plantas. Sin embargo, todavía no está claro el potencial de que estos efectos estresantes subletales sobre las interacciones planta-polinizador a nivel individual escalen a cambios en las dinámicas de las plantas y las poblaciones silvestres de polinizadores a nivel de sistema. Desarrollamos un modelo basado en el agente y con parámetros empíricos para un sistema de polinización de abejorros llamado SimBee. Con él analizamos los efectos de las disminuciones inducidas por estresantes sobre la capacidad de memoria y la velocidad de procesamiento de información de los forrajeros individuales en la abundancia de abejas (escenario 1), diversidad de plantas (escenario 2) y la estabilidad en el sistema abeja-planta (escenario 3) durante 20 temporadas virtuales. El modelado de una red simple de polinización de un abejorro y cuatro especies de plantas con floración a la par y polinizadas por abejas indicó que la declinación de abejas y los eventos de extinción de plantas podrían ocurrir cuando sólo el 25% de la población forrajera muestra daños cognitivos. Los porcentajes más altos de daños cognitivos mostraron 50% de pérdida de abejas en sólo cinco temporadas virtuales y eventos de extinción en todo el sistema en <20 temporadas virtuales bajo algunas condiciones. La extinción de las especies de plantas ocurrió sin importar el tamaño poblacional de las abejas, lo que indica que los cambios inducidos por los estresantes tan sólo al comportamiento polinizador podrían resultar en la pérdida de especies dentro de las comunidades botánicas. Estos resultados indican que los efectos estresantes subletales en los mecanismos de comportamiento de los polinizadores, aunque parezcan insignificantes a nivel de individuo, tienen el potencial acumulativo, en principio, de degradar las interacciones entre especies de plantas y polinizadores a nivel de sistema. Nuestro trabajo resalta la importancia de una estrategia de modelado basado en el agente para la identificación y mitigación de los impactos antropogénicos sobre los sistemas planta-polinizador.

Adaptive Foraging of Pollinators Can Promote Pollination of a Rare Plant Species.

Most pollinators have the foraging flexibility to visit a wide variety of plant species. Yet few studies of pollinator-mediated processes in plants have considered the effects of variation in individual foraging patterns on plant reproductive success. In this study, we use an individual-based model of pollinator foraging economics to predict how visitation rates and pollination success of two coflowering plant species change with their frequency (relative abundance). Whereas previous studies suggested that adaptive foraging of pollinators always favors pollination of abundant plant species (positive frequency dependence), here we show that under certain conditions the per capita pollination success of a rare plant species can exceed that of a more abundant species. Specifically, when the overall flower density is sufficiently high and pollinators' perception ranges are sufficiently large, animals with limited memory of previously encountered rewards forage in a way that favors pollination of the rarer plant species. Moreover, even with perfectly informed foragers, a rare plant species benefits more from offering a higher floral reward than a more abundant species. Our results show that adaptive foraging of individual pollinators can have important implications for plant community dynamics and the persistence of rare plant species.

"Hummingbird" floral traits interact synergistically to discourage visitation by bumble bee foragers.

Pollination syndromes are suites of floral traits presumed to reflect adaptations to attract and utilize a "primary" type of animal pollinator. However, syndrome traits may also function to deter "secondary" flower visitors that reduce plant fitness through their foraging activities. Here we use the hummingbird-pollinated plant species Mimulus cardinalis as a model to investigate the potential deterrent effects of classic bird syndrome traits on bumble bee foragers. To establish that M. cardinalis flowers elicit an avoidance response in bees, we assessed the choice behavior of individual foragers on a mixed experimental array of M. cardinalis and its bee-pollinated sister species M. lewisii. As expected, bees showed a strong preference against M. cardinalis flowers (only 22% of total bee visits were to M. cardinalis), but surprisingly also showed a high degree of individual specialization (95.2% of total plant transitions were between conspecifics). To determine M. cardinalis floral traits that discourage bee visitation, we then assessed foraging responses of individuals to M. cardinalis-like and M. lewisii-like floral models differing in color, orientation, reward, and combinations thereof. Across experiments, M. cardinalis-like trait combinations consistently produced a higher degree of flower avoidance behavior and individual specialization than expected based on bee responses to each trait in isolation. We then conducted a series of flower discrimination experiments to assess the ability of bees to utilize traits and trait combinations associated with each species. Relative to M. lewisii-like alternatives, M. cardinalis-like traits alone had a minimal effect on bee foraging proficiency but together increased the time bees spent searching for rewarding flowers from 1.49 to 2.65 s per visit. Collectively, our results show that M. cardinalis flowers impose foraging costs on bumble bees sufficient to discourage visitation and remarkably, generate such costs through synergistic color-orientation and color-reward trait interactions. Floral syndromes therefore represent complex adaptations to multiple pollinator groups, rather than simply the primary pollinator.

Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism.

Understanding the biophysical basis of animal magnetoreception has been one of the greatest challenges in sensory biology. Recently it was discovered that the light-dependent magnetic sense of Drosophila melanogaster is mediated by the ultraviolet (UV)-A/blue light photoreceptor cryptochrome (Cry). Here we show, using a transgenic approach, that the photoreceptive, Drosophila-like type 1 Cry and the transcriptionally repressive, vertebrate-like type 2 Cry of the monarch butterfly (Danaus plexippus) can both function in the magnetoreception system of Drosophila and require UV-A/blue light (wavelength below 420 nm) to do so. The lack of magnetic responses for both Cry types at wavelengths above 420 nm does not fit the widely held view that tryptophan triad-generated radical pairs mediate the ability of Cry to sense a magnetic field. We bolster this assessment by using a mutant form of Drosophila and monarch type 1 Cry and confirm that the tryptophan triad pathway is not crucial in magnetic transduction. Together, these results suggest that animal Crys mediate light-dependent magnetoreception through an unconventional photochemical mechanism. This work emphasizes the utility of Drosophila transgenesis for elucidating the precise mechanisms of Cry-mediated magnetosensitivity in insects and also in vertebrates such as migrating birds.

Cryptochrome mediates light-dependent magnetosensitivity in Drosophila.

Although many animals use the Earth's magnetic field for orientation and navigation, the precise biophysical mechanisms underlying magnetic sensing have been elusive. One theoretical model proposes that geomagnetic fields are perceived by chemical reactions involving specialized photoreceptors. However, the specific photoreceptor involved in such magnetoreception has not been demonstrated conclusively in any animal. Here we show that the ultraviolet-A/blue-light photoreceptor cryptochrome (Cry) is necessary for light-dependent magnetosensitive responses in Drosophila melanogaster. In a binary-choice behavioural assay for magnetosensitivity, wild-type flies show significant naive and trained responses to a magnetic field under full-spectrum light ( approximately 300-700 nm) but do not respond to the field when wavelengths in the Cry-sensitive, ultraviolet-A/blue-light part of the spectrum (<420 nm) are blocked. Notably, Cry-deficient cry(0) and cry(b) flies do not show either naive or trained responses to a magnetic field under full-spectrum light. Moreover, Cry-dependent magnetosensitivity does not require a functioning circadian clock. Our work provides, to our knowledge, the first genetic evidence for a Cry-based magnetosensitive system in any animal.

Exploring the Role of Cognition in the Annual Fall Migration of the Monarch Butterfly (Danaus plexippus).

Each fall, monarch butterflies in eastern North America undergo an extraordinary long-distance migration to wintering areas in central Mexico, where they remain until returning northward in the spring. Migrants survive the overwintering period by metabolizing lipid reserves accumulated exclusively though floral nectar; however, there is little known about how individuals maximize foraging efficiency in the face of floral environments that constantly change in complex and unpredictable ways along their migratory route. Here, a proboscis extension paradigm is used to investigate the role of cognition during the foraging phase of monarch migration. Male and female migratory butterflies were consecutively trained to discriminate between two color and odor cues and then tested for their ability to simultaneously retain the information on the reward value of each cue in memory without reinforcement over a period of 7 days. To gain further insight into cognitive abilities of monarchs as a migratory species, a second set of captive-reared males and females were tested under harnessed conditions at the same time as wild-caught fall migrants. Results showed that male and female migrants can learn the reward properties of color and odor cues with over 75% accuracy after less than 40 s of exposure and can simultaneously retain visual and olfactory information predicting the availability of floral rewards in memory without reinforcement for at least 7 days. Captive-reared male butterflies also showed the ability to retain visual and olfactory information in long-term memory for 7 days; however, 80% of captive-reared females could not retain color cues in long-term memory for more than 24 h. These novel findings are consistent with the view that monarch butterflies, as a migratory species, have enhancements to long-term memory that enable them to minimize the amount of time and energy wasted searching for suitable nectar sources during their annual fall migration, thereby optimizing migratory performance and increasing the chance of overwinter survival. The possibility that female monarchs undergo a seasonal change in visual long-term memory warrants further empirical investigation.

Distinct neuropeptide-receptor modules regulate a sex-specific behavioral response to a pheromone.

Dioecious species are a hallmark of the animal kingdom, with opposing sexes responding differently to identical sensory cues. Here, we study the response of C. elegans to the small-molecule pheromone, ascr#8, which elicits opposing behavioral valences in each sex. We identify a novel neuropeptide-neuropeptide receptor (NP/NPR) module that is active in males, but not in hermaphrodites. Using a novel paradigm of neuropeptide rescue that we established, we leverage bacterial expression of individual peptides to rescue the sex-specific response to ascr#8. Concurrent biochemical studies confirmed individual FLP-3 peptides differentially activate two divergent receptors, NPR-10 and FRPR-16. Interestingly, the two of the peptides that rescued behavior in our feeding paradigm are related through a conserved threonine, suggesting that a specific NP/NPR combination sets a male state, driving the correct behavioral valence of the ascr#8 response. Receptor expression within pre-motor neurons reveals novel coordination of male-specific and core locomotory circuitries.

Defining behavioral and molecular differences between summer and migratory monarch butterflies.

BACKGROUND: In the fall, Eastern North American monarch butterflies (Danaus plexippus) undergo a magnificent long-range migration. In contrast to spring and summer butterflies, fall migrants are juvenile hormone deficient, which leads to reproductive arrest and increased longevity. Migrants also use a time-compensated sun compass to help them navigate in the south/southwesterly direction en route for Mexico. Central issues in this area are defining the relationship between juvenile hormone status and oriented flight, critical features that differentiate summer monarchs from fall migrants, and identifying molecular correlates of behavioral state. RESULTS: Here we show that increasing juvenile hormone activity to induce summer-like reproductive development in fall migrants does not alter directional flight behavior or its time-compensated orientation, as monitored in a flight simulator. Reproductive summer butterflies, in contrast, uniformly fail to exhibit directional, oriented flight. To define molecular correlates of behavioral state, we used microarray analysis of 9417 unique cDNA sequences. Gene expression profiles reveal a suite of 40 genes whose differential expression in brain correlates with oriented flight behavior in individual migrants, independent of juvenile hormone activity, thereby molecularly separating fall migrants from summer butterflies. Intriguing genes that are differentially regulated include the clock gene vrille and the locomotion-relevant tyramine beta hydroxylase gene. In addition, several differentially regulated genes (37.5% of total) are not annotated. We also identified 23 juvenile hormone-dependent genes in brain, which separate reproductive from non-reproductive monarchs; genes involved in longevity, fatty acid metabolism, and innate immunity are upregulated in non-reproductive (juvenile-hormone deficient) migrants. CONCLUSION: The results link key behavioral traits with gene expression profiles in brain that differentiate migratory from summer butterflies and thus show that seasonal changes in genomic function help define the migratory state.

Bumblebees learn to forage like Bayesians.

Bayesian foraging in patchy environments requires that foragers have information about the distribution of resources among patches (prior information), either set by natural selection or learned from past experience. We test the hypothesis that bumblebee foragers can rapidly learn prior information from past experience in two very different experimental environments. In the high-variance environment (patches of low and high quality), stochastic optimality models predicted that finding rewards should sometimes sharply increase an optimal forager's tendency to stay in a patch (an incremental response), whereas in the uniform environment, finding rewards should always decrease the tendency to stay (a decremental response). We use Cox regression models to show that, in a matter of hours, bees learned to match both predicted responses, resulting in a reward intake rate that averaged 80% of the predicted maximum. Following training in either environment, bees' adaptive behavior carried over to a common test environment, thus confirming the influence of memorized prior information. Although Bayesian foraging by learning is often presumed, this study is the first to clearly isolate the adaptive use of a learned prior expectation. More generally, it highlights the remarkable adaptive plasticity of an important generalist pollinator and agent of selection.

Immune-cognitive system connectivity reduces bumblebee foraging success in complex multisensory floral environments.

Bumblebees are declining at alarming rate worldwide, posing a significant threat to the function and diversity of temperate ecosystems. These declines have been attributed, in part, to the direct effect of specific pathogens on bumblebee survival. However, pathogens may also have a negative impact on host populations indirectly through immune-induced cognitive deficits in infected individuals. To gain greater insight into mechanisms and potential conservation implications of such 'immune-brain crosstalk' in bumblebees, we non-pathogenetically activated humoral and cellular immune pathways in individuals and then tested for long-term reductions in cognitive performance and foraging proficiency. We show that chronic activation of humoral, but not a cellular, immune pathways and effectors in foragers significantly reduces their ability to flexibly and efficiently harvest resources in multi-sensory floral environments for at least 7 days post-treatment. Humoral defense responses thus have the potential to confer significant foraging costs to bumblebee foragers over timeframes that would negatively impact colony growth and reproductive output under natural conditions. Our findings indicate that fitness effects of immune-brain crosstalk should be considered before attributing wild bumblebee decline to a particular pathogen species.

One size does not fit all: Caste and sex differences in the response of bumblebees (Bombus impatiens) to chronic oral neonicotinoid exposure.

Neonicotinoid insecticides have been implicated in the rapid global decline of bumblebees over recent years, particularly in agricultural and urban areas. While there is much known about neonicotinoid toxicity effects at the colony stage of the bumblebee annual cycle, far less is known about such effects at other stages critical for the maintenance of wild populations. In the present work, individual-based feeding assays were used to show that chronic consumption of the widely used neonicotinoid clothianidin at a field-realistic average rate of 3.6 and 4.0 ng/g·bee/day reduces survival of queen and male bumblebees, respectively, within a 7-day period. In contrast, worker survival was unaffected at a similar consumption rate of 3.9 ng/g·bee/day. To test the hypothesis that males have a lower tolerance for oral clothianidin exposure than workers due to their haploid genetic status, RNAseq analysis was used to compare the transcriptomic responses of workers and males to chronic intake of clothianidin at a sub-lethal dose of 0.37ng/bee/day for 5 days. Surprisingly, clothianidin consumption only altered the expression of 19 putative detoxification genes in a sex-specific manner, with 11/19 genes showing increased expression in workers. Sub-lethal clothianidin exposure also altered the expression of 40 genes associated with other major biological functions, including locomotion, reproduction, and immunity. Collectively, these results suggest that chronic oral toxicity effects of neonicotinoids are greatest during mating and nest establishment phases of the bumblebee life cycle. Chronic oral toxicity testing on males and queens is therefore required in order to fully assess the impact of neonicotinoids on wild bumblebee populations.

Ecological context influences pollinator deterrence by alkaloids in floral nectar.

Secondary compounds may benefit plants by deterring herbivores, but the presence of these defensive chemicals in floral nectar may also deter beneficial pollinators. This trade-off between sexual reproduction and defense has received minimal study. We determined whether the pollinator-deterring effects of a nectar alkaloid found in the perennial vine Gelsemium sempervirens depend on ecological context (i.e. the availability of alternative nectar sources) by monitoring the behavioural response of captive bumblebees (Bombus impatiens, an important pollinator of G. sempervirens in nature) to nectar alkaloids in several ecologically relevant scenarios. Although alkaloids in floral nectar tended to deter visitation by bumblebees, the magnitude of that effect depended greatly on the availability and nectar properties of alternative flowers. Ecological context should thus be considered when assessing ecological costs of plant defense in terms of pollination services. We consider adaptive strategies that would enable plants to minimize pollinator deterrence because of defensive compounds in flowers.

The birds, the bees, and the virtual flowers: can pollinator behavior drive ecological speciation in flowering plants?

Biologists have long assumed that pollinator behavior is an important force in angiosperm speciation, yet there is surprisingly little direct evidence that floral preferences in pollinators can drive floral divergence and the evolution of reproductive (ethological) isolation between incipient plant species. In this study, we expose computer-generated plant populations with a wide variation in flower color to selection by live and virtual hummingbirds and bumblebees and track evolutionary changes in flower color over multiple generations. Flower color, which was derived from the known genetic architecture and phenotypic variance of naturally occurring plant species pollinated by both groups, evolved in simulations through a genetic algorithm in which pollinator preference determined changes in flower color between generations. The observed preferences of live hummingbirds and bumblebees were strong enough to cause adaptive divergence in flower color between plant populations but did not lead to ethological isolation. However, stronger preferences assigned to virtual pollinators in sympatric and allopatric scenarios rapidly produced ethological isolation. Pollinators can thus drive ecological speciation in flowering plants, but more rigorous and comprehensive behavioral studies are required to specify conditions that produce sufficient preference levels in pollinators.

Habitat assessment ability of bumble-bees implies frequency-dependent selection on floral rewards and display size.

Foraging pollinators could visit hundreds of flowers in succession on mass-flowering plants, yet they often visit only a small number--potentially saving the plant from much self-pollination among its own flowers (geitonogamy). This study tests the hypothesis that bumble-bee (Bombus impatiens) residence on a particular plant depends on an assessment of that plant's reward value relative to the overall quality experienced in the habitat. In a controlled environment, naive bees were given experience in a particular habitat (all plants having equal nectar quality or number of rewarding flowers), and we tested whether they learn about and adaptively exploit a new habitat type. Bees' residence on a plant (number of flowers probed per visit) was eventually invariant to a doubling of absolute nectar quality and increased only slightly with a doubling of absolute flower number in the habitat. These results help to explain why pollinators are quick to leave highly rewarding plants and suggest that the fitness of rewarding plant traits will often be frequency dependent. One implication is that geitonogamy may be a less significant constraint on the evolution of rewarding traits than generally supposed.

Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information.

Parasitic infection can influence a variety of behavioural mechanisms in animals, but little is known about the effects of infection on the cognitive processes underlying ecologically relevant behaviours. Here, we examined whether parasitic infection alters cognitive aspects of foraging in a social insect, the bumble-bee (Bombus impatiens). In controlled experiments, we assessed the ability of foraging bees to discriminate rewarding from non-rewarding flowers on the basis of colour and odour. We found that natural and experimental infection by a protozoan parasite (Crithidia bombi, which lives exclusively within the gut tract), impaired the ability of foragers to learn the colour of rewarding flowers. Parasitic infection can thus disrupt central nervous system pathways that mediate cognitive processes in bumble-bees and as a consequence, can reduce their ability to monitor floral resources and make economic foraging decisions. It is postulated that this infection-induced change to cognitive function in bumble-bees is the result of communication between immune and nervous systems. Parasitized animals, including invertebrates, can therefore show subtle behavioural changes that are nonetheless ecologically significant and reflect complex mechanisms.

A magnetic compass aids monarch butterfly migration.

Convincing evidence that migrant monarch butterflies (Danaus plexippus) use a magnetic compass to aid their fall migration has been lacking from the spectacular navigational capabilities of this species. Here we use flight simulator studies to show that migrants indeed possess an inclination magnetic compass to help direct their flight equatorward in the fall. The use of this inclination compass is light-dependent utilizing ultraviolet-A/blue light between 380 and 420 nm. Notably, the significance of light <420 nm for inclination compass function was not considered in previous monarch studies. The antennae are important for the inclination compass because they appear to contain light-sensitive magnetosensors. For migratory monarchs, the inclination compass may serve as an important orientation mechanism when directional daylight cues are unavailable and may also augment time-compensated sun compass orientation for appropriate directionality throughout the migration.

Discordant timing between antennae disrupts sun compass orientation in migratory monarch butterflies.

To navigate during their long-distance migration, monarch butterflies (Danaus plexippus) use a time-compensated sun compass. The sun compass timing elements reside in light-entrained circadian clocks in the antennae. Here we show that either antenna is sufficient for proper time compensation. However, migrants with either antenna painted black (to block light entrainment) and the other painted clear (to permit light entrainment) display disoriented group flight. Remarkably, when the black-painted antenna is removed, re-flown migrants with a single, clear-painted antenna exhibit proper orientation behaviour. Molecular correlates of clock function reveal that period and timeless expression is highly rhythmic in brains and clear-painted antennae, while rhythmic clock gene expression is disrupted in black-painted antennae. Our work shows that clock outputs from each antenna are processed and integrated together in the monarch time-compensated sun compass circuit. This dual timing system is a novel example of the regulation of a brain-driven behaviour by paired organs.

Human cryptochrome exhibits light-dependent magnetosensitivity.

Humans are not believed to have a magnetic sense, even though many animals use the Earth's magnetic field for orientation and navigation. One model of magnetosensing in animals proposes that geomagnetic fields are perceived by light-sensitive chemical reactions involving the flavoprotein cryptochrome (CRY). Here we show using a transgenic approach that human CRY2, which is heavily expressed in the retina, can function as a magnetosensor in the magnetoreception system of Drosophila and that it does so in a light-dependent manner. The results show that human CRY2 has the molecular capability to function as a light-sensitive magnetosensor and reopen an area of sensory biology that is ready for further exploration in humans.

Navigational mechanisms of migrating monarch butterflies.

Recent studies of the iconic fall migration of monarch butterflies have illuminated the mechanisms behind their southward navigation while using a time-compensated sun compass. Skylight cues, such as the sun itself and polarized light, are processed through both eyes and are probably integrated in the brain's central complex, the presumed site of the sun compass. Time compensation is provided by circadian clocks that have a distinctive molecular mechanism and that reside in the antennae. Monarchs might also use a magnetic compass because they possess two cryptochromes that have the molecular capability for light-dependent magnetoreception. Multiple genomic approaches are now being used with the aim of identifying navigation genes. Monarch butterflies are thus emerging as an excellent model organism in which to study the molecular and neural basis of long-distance migration.

Antennal circadian clocks coordinate sun compass orientation in migratory monarch butterflies.

During their fall migration, Eastern North American monarch butterflies (Danaus plexippus) use a time-compensated Sun compass to aid navigation to their overwintering grounds in central Mexico. It has been assumed that the circadian clock that provides time compensation resides in the brain, although this assumption has never been examined directly. Here, we show that the antennae are necessary for proper time-compensated Sun compass orientation in migratory monarch butterflies, that antennal clocks exist in monarchs, and that they likely provide the primary timing mechanism for Sun compass orientation. These unexpected findings pose a novel function for the antennae and open a new line of investigation into clock-compass connections that may extend widely to other insects that use this orientation mechanism.