COLLABORATIVE RESEARCH: Novel mechanisms of mate localization in plant-dwelling insects: an integration of behavior, neurobiology and biomechanics.
Plant-feeding insects are among the most abundant and diverse organisms on earth, with a major impact on both natural ecosystems and agriculture. For many of these insects, survival and reproduction depend on the detection of low-amplitude vibrations of the plant surface, generated by the activity of potential mates, competitors, or natural enemies. However, in spite of the importance of plant-borne vibrations for insect behavior and ecology, two fundamental questions remain unanswered. First, how can a small insect determine the direction of a vibration source elsewhere on the same plant? And second, can an insect use the complex motion of plant stems and leaves during vibration transmission to estimate its distance from the source? To answer these questions, an interdisciplinary team has been assembled with expertise in behavior, neurobiology, mechanical engineering, and computational modeling. The team will develop new research tools and use them to understand how insect behavior is guided by mechanical vibrations, using computational models to integrate the results of behavioral experiments, sensory neurophysiology, and biomechanical measurements. Previous research by this team has revealed surprising sources of information that insects may use in sensing; for example, the motion of an insect body, resting on its six legs, can be highly sensitive to the direction of travel of a plant-borne vibration. Results of the proposed research will transform the current understanding of how mechanical vibrations influence the behavior of one of the most ecologically and economically important groups of organisms. Broader impacts: Because collaborative teamwork is increasingly important for scientific progress, a major goal of the project will be to train graduate students in the skills needed for a career in interdisciplinary research. Finally, insights gained during the study could lead to the design of directional vibration sensors that could have an impact on many industries.
This project investigated how small insects solve a difficult sensing problem: finding the source of a substrate-borne vibration. Because insects must solve such problems on a micro scale with relatively simple nervous systems, their solutions can suggest new approaches for man-made directional sensors. In addition to the human interest in measuring vibrations traveling through the ground and through structures, many species of insects and other organisms use substrate-borne vibrations to communicate, to find prey, or to avoid predators. Accordingly, this little-studied form of information exchange is important for understanding many ecological and social interactions in nature. Identifying how insects solve this directional sensing problem requires a collaborative approach, and the research team for this project included a behavioral ecologist, a neurophysiologist, and a mechanical engineer. The study species were two small insect species that use plant-borne vibrations to communicate. Their behavior provides a robust assay of directional ability, because mate-searching males home in on vibrational signals produced by the female. Females mate with the first male to arrive, so localization is a competitive race. Males walk along the plant stem and stop periodically to signal and elicit a female reply: the decision points are thus easily identified, allowing us to measure the vibrational inputs and relate them to directional decisions. The first step was to characterize the two-dimensional substrate motion experienced by the insects, and to relate the characteristics of those vibrations to the insects’ success in making accurate directional decisions (i.e., to move forward to reverse direction along a plant stem). This step showed that the insects do face a daunting sensory problem: the wavelengths are much longer than the distance between the sensors in the insects’ front and back legs, the vibrations travel at very different speeds at different locations, and searching individuals must navigate the complex, branching structure of the plant. Nevertheless, the insects solved this sensing problem. Their decisions were based primarily on the direction of wave propagation, strongly suggesting that the insects are capable of directional sensing based on sampling at a single location. Furthermore, we showed for the first time that the two-dimensional motion of the stem is important for localization: the insects made more accurate decisions when the direction of stem motion was aligned with the long axis of the legs, the axis along which their vibration detectors are most sensitive. Because localization of a female on a plant could potentially rely on multiple cues (locations on the plant where females typically occur, direction of wave propagation, and a gradient of lower to higher amplitude), the next step was to design controlled experiments to test individual cues. We showed for the first time that the insects’ decisions are strongly influenced by changes in amplitude, such that they follow a gradient of increasing signal strength. However, amplitude changes accounted for only a small minority of decisions made by searching insects, leaving point-source directional sensing as the primary mechanism. However, the time delays are extremely short between vibration detectors in front and back legs; so how can the insects extract the directional information they need? Previous work by this research team suggested a novel mechanism of vibration localization: the motion of the insects’ bodies, resting on six legs and driven by a substrate vibration, is itself highly directional. For example, when the vibration arrives from behind the insect, the back of its body moves much more than the front. Testing whether the insects actually make use of this biomechanical source of information required neurophysiological measurements. In general, latency -- the delay between the stimulus and the nerve response – is shorter for higher-amplitude stimuli. The ‘mechanical directionality’ hypothesis thus predicted that latencies in the front and back legs would differ depending on the direction of the vibration. Measurements of the timing of nerve responses when the insects were on a device designed to replicate vibration transmission showed that this prediction was met: there were direction-dependent differences in latency between front and back legs. The mechanical response of the insects’ body to substrate vibration thus transforms time differences too small to be resolved by the nervous system, into differences in the motion of the front and back of the body, which in turn causes substantial differences in the timing of when nerves begin to fire in the front and back legs. Engineering students are currently studying this mechanism of directional localization. This research was the topic of one PhD dissertation and one MS thesis. Presentation of the results at an international conference led to an edited volume entitled ‘Studying Vibrational Communication’, now in press, which promotes research in this field. The hidden world of insect vibrational communication was the subject of multiple presentations to college classes and two documentary films.
