About

Stacey A. Combes is a Professor in the Department of Neurobiology, Physiology and Behavior at the University of California, Davis. Her research focuses on the biomechanics and behavioral ecology of flying insects, with particular attention to wing biomechanics, flight in complex environments, and the behavior of flying insects. She leads the Combes Lab, which investigates these areas through interdisciplinary approaches combining neurobiology, physiology, and behavior. The lab includes graduate students from the Animal Behavior and Neuroscience graduate groups, as well as undergraduate research assistants from various biological sciences disciplines. Professor Combes' work contributes to understanding the physical and behavioral mechanisms that enable insect flight, which has implications for fields ranging from ecology to robotics.

Research topics

• Engineering
• Aerospace engineering
• Physics
• Geography
• Biology
• Environmental science
• Computer Science
• Ecology
• Mechanics
• Statistics
• Classical mechanics
• Psychology
• Acoustics
• Meteorology
• Mathematics
• Communication
• Human–computer interaction
• Geodesy

Selected publications

• Flying, nectar-loaded honey bees conserve water and improve heat tolerance by reducing wingbeat frequency and metabolic heat production

  Proceedings of the National Academy of Sciences · 2024-01-16 · 22 citations

  articleOpen access

  Heat waves are becoming increasingly common due to climate change, making it crucial to identify and understand the capacities for insect pollinators, such as honey bees, to avoid overheating. We examined the effects of hot, dry air temperatures on the physiological and behavioral mechanisms that honey bees use to fly when carrying nectar loads, to assess how foraging is limited by overheating or desiccation. We found that flight muscle temperatures increased linearly with load mass at air temperatures of 20 or 30 °C, but, remarkably, there was no change with increasing nectar loads at an air temperature of 40 °C. Flying, nectar-loaded bees were able to avoid overheating at 40 °C by reducing their flight metabolic rates and increasing evaporative cooling. At high body temperatures, bees apparently increase flight efficiency by lowering their wingbeat frequency and increasing stroke amplitude to compensate, reducing the need for evaporative cooling. However, even with reductions in metabolic heat production, desiccation likely limits foraging at temperatures well below bees' critical thermal maxima in hot, dry conditions.

  PublisherOA PDFDOI

• Multimodal processing of noisy cues in bumblebees

  iScience · 2023-11-25 · 6 citations

  articleOpen accessSenior author

  Multimodal cues can improve behavioral responses by enhancing the detection and localization of sensory cues and reducing response times. Across species, studies have shown that multisensory integration of visual and olfactory cues can improve response accuracy. However, in real-world settings, sensory cues are often noisy; visual and olfactory cues can be deteriorated, masked, or mixed, making the target cue less clear to the receiver. In this study, we use an associative learning paradigm (Free Moving Proboscis Extension Reflex, FMPER) to show that having multimodal cues may improve the accuracy of bees' responses to noisy cues. Adding a noisy visual cue improves the accuracy of response to a noisy olfactory cue, despite neither the clear nor noisy visual cue being sufficient when paired with a novel olfactory cue. This may provide insight into the neural mechanisms underlying multimodal processing and the effects of environmental change on pollination services.

  PublisherDOI

• Complex hemolymph circulation patterns in grasshopper wings

  Communications Biology · 2023-03-23 · 17 citations

  articleOpen accessSenior author

  An insect's living systems-circulation, respiration, and a branching nervous system-extend from the body into the wing. Wing hemolymph circulation is critical for hydrating tissues and supplying nutrients to living systems such as sensory organs across the wing. Despite the critical role of hemolymph circulation in maintaining healthy wing function, wings are often considered "lifeless" cuticle, and flows remain largely unquantified. High-speed fluorescent microscopy and particle tracking of hemolymph in the wings and body of the grasshopper Schistocerca americana revealed dynamic flow in every vein of the fore- and hindwings. The global system forms a circuit, but local flow behavior is complex, exhibiting three distinct types: pulsatile, aperiodic, and "leaky" flow. Thoracic wing hearts pull hemolymph from the wing at slower frequencies than the dorsal vessel; however, the velocity of returning hemolymph (in the hindwing) is faster than in that of the dorsal vessel. To characterize the wing's internal flow mechanics, we mapped dimensionless flow parameters across the wings, revealing viscous flow regimes. Wings sustain ecologically important insect behaviors such as pollination and migration. Analysis of the wing circulatory system provides a template for future studies investigating the critical hemodynamics necessary to sustaining wing health and insect flight.

  PublisherOA PDFDOI

• Close encounters of three kinds: impacts of leg, wing and body collisions on flight performance in carpenter bees

  Journal of Experimental Biology · 2023-04-17 · 5 citations

  articleOpen accessSenior author

  Flying insects often forage among cluttered vegetation that forms a series of obstacles in their flight path. Recent studies have focused on behaviors needed to navigate clutter while avoiding all physical contact and, as a result, we know little about flight behaviors that do involve encounters with obstacles. Here, we challenged carpenter bees (Xylocopa varipuncta) to fly through narrow gaps in an obstacle course to determine the kinds of obstacle encounters they experience, as well as the consequences for flight performance. We observed three kinds of encounters: leg, body and wing collisions. Wing collisions occurred most frequently (in about 40% of flights, up to 25 times per flight) but these had little effect on flight speed or body orientation. In contrast, body and leg collisions, which each occurred in about 20% of flights (1-2 times per flight), resulted in decreased flight speeds and increased rates of body rotation (yaw). Wing and body collisions, but not leg collisions, were more likely to occur in wind versus still air. Thus, physical encounters with obstacles may be a frequent occurrence for insects flying in some environments, and the immediate effects of these encounters on flight performance depend on the body part involved.

  PublisherOA PDFDOI

• Going against the flow: bumblebees prefer to fly upwind and display more variable kinematics when flying downwind

  Journal of Experimental Biology · 2023-04-18 · 6 citations

  articleOpen access1st authorCorresponding

  Foraging insects fly over long distances through complex aerial environments, and many can maintain constant ground speeds in wind, allowing them to gauge flight distance. Although insects encounter winds from all directions in the wild, most lab-based studies have employed still air or headwinds (i.e. upwind flight); additionally, insects are typically compelled to fly in a single, fixed environment, so we know little about their preferences for different flight conditions. We used automated video collection and analysis methods and a two-choice flight tunnel paradigm to examine thousands of foraging flights performed by hundreds of bumblebees flying upwind and downwind. In contrast to the preference for flying with a tailwind (i.e. downwind) displayed by migrating insects, we found that bees prefer to fly upwind. Bees maintained constant ground speeds when flying upwind or downwind in flow velocities from 0 to 2 m s-1 by adjusting their body angle, pitching down to raise their air speed above flow velocity when flying upwind, and pitching up to slow down to negative air speeds (flying backwards relative to the flow) when flying downwind. Bees flying downwind displayed higher variability in body angle, air speed and ground speed. Taken together, bees' preference for upwind flight and their increased kinematic variability when flying downwind suggest that tailwinds may impose a significant, underexplored flight challenge to bees. Our study demonstrates the types of questions that can be addressed with newer approaches to biomechanics research; by allowing bees to choose the conditions they prefer to traverse and automating filming and analysis to examine massive amounts of data, we were able to identify significant patterns emerging from variable locomotory behaviors, and gain valuable insight into the biomechanics of flight in natural environments.

  PublisherOA PDFDOI

• Autonomous Expansion of Grasshopper Wings Reveals External Forces Contribute to Final Adult Wing Shape

  Integrative and Comparative Biology · 2023-09-15 · 4 citations

  articleSenior author

  Ecdysis, transformation from juvenile to adult form in insects, is time-consuming and leaves insects vulnerable to predation. For winged insects, the process of wing expansion during ecdysis, unfurling and expanding the wings, is a critical bottleneck in achieving sexual maturity. Internal and external forces play a role in wing expansion. Vigorous abdominal pumping during wing expansion allows insects to pressurize and inflate their wings, filling them with hemolymph. In addition, many insects adopt expansion-specific postures and, if inhibited, do not expand their wings normally, suggesting that external forces such as gravity may play a role. However, two previous studies over 40 years ago, reported that the forewings of swarming locusts can expand autonomously when removed from the emerging insect and laid flat on a saline solution. Termed "autoexpansion," we replicated previous experiments of autoexpansion on flat liquid media, documenting changes in both wing length and area over time while also focusing on the role of gravity in autoexpansion. Using the North American bird grasshopper Schistocerca americana, we tested four autoexpansion treatments of varying surface tension and hydrophobicity (gravity, deionized water, buffer, and mineral oil) while simultaneously observing and measuring intact, normal wing expansion. Finally, we constructed a simple model of a viscoelastic expanding wing subjected to gravity, to determine whether it could capture aspects of wing expansion. Our data confirmed that wing autoexpansion does occur in S. americana, but autoexpanding wings, especially hindwings, failed to increase to the same final length and area as intact wings. We found that gravity plays an important role in wing expansion, early in the expansion process. Combined with the significant mass increase we documented in intact wings, it suggests that hydraulic pumping of hemolymph into the wings plays an important role in increasing the area of expanding wings, especially in driving expansion of the large, pleated hindwings. Autoexpansion in a non-swarming orthopteran suggests that local cues driving wing autoexpansion may serve a broader purpose, reducing total expansion time and costs by shifting some processes from central to local control. Documenting wing autoexpansion in a widely studied model organism and demonstrating a mathematical model provides a tractable new system for exploring higher level questions about the mechanisms of wing expansion and the implications of autoexpansion, as well as potential bioinspiration for future technologies applicable to micro-air vehicles, space exploration, or medical and prosthetic devices.

  PublisherDOI

• A critique of common methods for comparing the scaling of vertical force production in flying insects

  bioRxiv (Cold Spring Harbor Laboratory) · 2022-02-13

  preprintOpen accessSenior author

  Abstract Maximum vertical force production (F vert ) is an integral measure of flight performance that generally scales with size. Numerous methods of measuring F vert and body size exist, but few studies have compared how these methods affect the conclusions of scaling analyses. We compared two common techniques for measuring F vert in bumblebees ( Bombus impatiens ) and mason bees ( Osmia lignaria ), and examined F vert scaling using five size metrics. F vert results were similar with incremental or asymptotic load-lifting, but scaling analyses were sensitive to the size metric used. Analyses based on some size metrics indicated similar scaling exponents and coefficients between species, whereas other metrics indicated different coefficients. Furthermore, F vert showed isometry with body lengths and fed and starved masses, but negative allometry with dry mass. We conclude that F vert can be measured using either incremental or asymptotic loading but choosing a size metric for scaling studies requires careful consideration.

  PublisherOA PDFDOI

• An evaluation of common methods for comparing the scaling of vertical force production in flying insects

  Current Research in Insect Science · 2022-01-01 · 1 citations

  articleOpen accessSenior author

  Maximum vertical force production (Fvert) is an integral measure of flight performance that generally scales with size. Numerous methods of measuring Fvert and body size are accessible to entomologists, but we do not know whether method selection affects inter- and intraspecific comparisons of Fvert-size scaling. We compared two common techniques for measuring Fvert in bumblebees (Bombus impatiens) and mason bees (Osmia lignaria), and examined Fvert scaling using five size metrics. Fvert results were similar with incremental or asymptotic load-lifting, but scaling analyses were sensitive to the size metric used. Analyses based on some size metrics indicated similar scaling exponents and coefficients between species, whereas other metrics indicated coefficients that differed by up to 18%. Furthermore, Fvert showed isometry with body lengths and fed and starved masses, but negative allometry with dry mass. We conclude that Fvert can be measured using either incremental or asymptotic loading but choosing a size metric for scaling studies requires careful consideration.

  PublisherDOI

• Wind and route choice affect performance of bees flying above versus within a cluttered obstacle field

  PLoS ONE · 2022-03-24 · 17 citations

  articleOpen accessSenior author

  Bees flying through natural landscapes frequently encounter physical challenges, such as wind and cluttered vegetation, but the influence of these factors on flight performance remains unknown. We analyzed 548 videos of wild-caught honeybees (Apis mellifera) flying through an enclosure containing a field of vertical obstacles that bees could choose to fly within (through open corridors, without maneuvering) or above. We varied obstacle field height and wind condition (still, headwinds or tailwinds), and examined how these factors affected bees' flight altitude, ground speed, and side-to-side casting motions (lateral excursions). When obstacle fields were short, bees flew at altitudes near the midpoint between the tunnel floor and ceiling. When obstacle fields approached or exceeded this midpoint, bees tended to increase their altitude, but they did not always avoid flying through obstacles, despite having the freedom to do so. Bees that flew above the obstacles exhibited 40% faster ground speeds and 36% larger lateral excursions than bees that flew within the obstacle fields. Wind did not affect flight altitude, but bees flew 12-19% faster in tailwinds, and their lateral excursions were 19% larger when flying in headwinds or tailwinds, as compared to still air. Our results show that bees flying through complex environments display flexibility in their route choices (i.e., flying above obstacles in some trials and through them in others), which affects their overall flight performance. Similar choices in natural landscapes could have broad implications for foraging efficiency, pollination, and mortality in wild bees.

  PublisherOA PDFDOI

• Close encounters of three kinds: impacts of leg, wing, and body collisions on flight performance in carpenter bees

  bioRxiv (Cold Spring Harbor Laboratory) · 2022-10-24

  preprintOpen accessSenior author

  Abstract Flying insects often forage among cluttered vegetation that forms a series of obstacles in their flight path. Recent studies have focused on behaviors needed to navigate clutter while avoiding all physical contact, and as a result, we know little about flight behaviors that do involve encounters with obstacles. Here, we challenged carpenter bees ( Xylocopa varipuncta ) to fly through narrow gaps in an obstacle course to determine the kinds of obstacle encounters they experience, as well as the consequences for flight performance. We observed three kinds of encounters: leg, body, and wing collisions. Wing collisions occurred most frequently (in about 40% of flights, up to 25 times per flight) but these had little effect on flight speed or body orientation. In contrast, body and leg collisions, which each occurred in about 20% of flights (1-2 times per flight), resulted in decreased flight speeds and increased rates of body rotation (yaw). Wing and body collisions, but not leg collisions, were more likely to occur in wind versus still air. Thus, physical encounters with obstacles may be a frequent occurrence for insects flying in some environments, and the immediate effects of these encounters on flight performance depends on the body part involved.

  PublisherOA PDFDOI

Recent grants

• CAREER: Insect Flight in Turbulent Environments

  NSF · $320k · 2016–2019

• Testing Structure/Function Relationships in an Ecological Context: Integration of Biomechanics, Behavior and Performance during Aerial Predation in Dragonflies

  NSF · $286k · 2010–2013

• Collaborative Research: Testing the consequences of wing flexibility to comprehensive flight performance in freely flying insects

  NSF · $521k · 2019–2024

• CAREER: Insect Flight in Turbulent Environments

  NSF · $614k · 2013–2016

Frequent coauthors

• James D. Crall

  University of Wisconsin–Madison

  25 shared

• Thierry Gidenne

  Institut National de la Recherche Agronomique du Niger

  16 shared

• Sridhar Ravi

  UNSW Sydney

  16 shared

• Nick Gravish

  University of California, San Diego

  13 shared

• Mary K. Salcedo

  Cornell University

  12 shared

• Naomi E. Pierce

  Harvard University

  12 shared

• Callin M. Switzer

  University of Washington

  11 shared

• Andrew Mountcastle

  Bates College

  11 shared

Labs

• The Combes LabPI