Infrasonic hearing in birds review

I’ve recently led a review paper on the subject of infrasonic hearing in birds, which is now published in Biological Reviews. The paper surveys the studies that have assessed infrasonic hearing in birds and presents various potential underlying anatomical and physiological traits that could be involved. In this post, I’ll summarize what I think are some of the interesting highlights from the review.

In terrestrial animals, hearing tests that go down to frequencies below 20 Hz (infrasound) are actually not all that common. However, the studies that we have available to date have demonstrated that a handful of mammals and birds can hear infrasound. Among bird species, infrasound sensitivity varies quite a bit. The rock dove and some birds in the order Galliformes (chicken, guinea fowl, and likely peafowl) are quite sensitive, while other birds such as budgerigar and mallard duck are quite insensitive. The infrasound sensitivity in the former group is in a similar range as those of mammals with excellent low frequency hearing abilities (elephants and black-tailed prairie dog).

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Rock dove, a bird known to detect infrasound (CC0 public domain image).

In nature, many of the sources of infrasound come from geophysical sources (e.g., colliding ocean waves, surf, earthquakes). One technical challenge that arises when interpreting the responses of freely behaving birds to natural infrasound sources is distinguishing a bird’s responses to infrasound from its responses to other concurrent non-acoustic fluctuations in atmospheric pressure. The non-acoustic pressure fluctuations (e.g., wind) can occur in the same frequency bands as infrasound, be of even greater magnitude than the infrasound, and can stimulate the ear. Laboratory tests are therefore an essential key to verify what birds can detect at infrasonic frequencies. We reviewed the different audiometry methods that have been used. Some of the more common methods have involved playback with subwoofers and training birds to recognize a sound, or presenting the sound through air volumes sealed over the eardrum and measuring neural responses.

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Budgerigar, a bird with poor sensitivity to infrasound (CC0 public domain image).

Which auditory mechanisms would promote the hearing of airborne infrasound? In general, the tympanic middle ear [i.e an eardrum and ear ossicle(s)] is quite important for detecting airborne sounds. Without the tympanic middle ear, hearing sensitivity to airborne sound is reduced significantly because a large portion of the sound reflects off the body surface. Therefore, having a middle ear that is very responsive at low frequencies is one major way that some birds could improve low-frequency hearing sensitivity. From theoretical work and studies in mammals, we know that this could be achieved by lowering the stiffness of the middle ear. This could be done by having larger cranial air cavities behind the eardrum and flexible ligaments attached to the ear ossicles. Large eardrums, which could resonate at lower frequencies, would also be beneficial (consider, for example, the ostrich, which has high middle ear vibrations at low frequencies).

In most birds, however, the middle ear vibrates maximally at relatively high frequencies, often at 2-5 kHz. As the frequency is lowered below this peak, middle ear vibration typically decreases approximately at a rate of 6 dB/octave (i.e., reduces by half every time the frequency is halved). At very low frequencies, the middle ear vibrations may decline to such low levels that alternative sound pathways to the ear should also be considered. We know that in animals lacking tympanic middle ears such as salamanders, snakes, and anurans, such ‘extratympanic’ pathways can dominate the auditory response at low frequencies. To demonstrate this possibility, we compared bird middle ear vibrations with vibrations from extratympanic body tissues, and presented a model for the vibrations for a solid sphere in a free field.

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Some of the bird ear structures considered in the context of infrasound perception (Figure 2 from the review).

The review next discusses mechanisms at the level of the inner ear and auditory receptors. We discuss how openings in the inner ear, such as the cochlear aqueduct and helicotrema, could affect how low frequencies are shunted within the inner ear. Neural recordings have indicated that the basilar papilla, the auditory end organ in birds, is responsive to infrasound in some species. It’s also plausible that vestibular organs could detect airborne infrasound, but this possibility has yet to be examined. For species that do respond well to infrasound, there are likely some specializations in the ‘electrical tuning’ of hair cells, in terms of the kinetics of the ion movement across the cell membranes, to allow the hair cell membrane potential to oscillate at very long periods.

Infrasonic hearing could be more widespread in birds and other terrestrial animals than is currently appreciated. This review should be a useful resource for future studies in this area. Check out the paper for all the details.

ZEYL, J.N., OUDEN, O. DEN, KÖPPL, C., ASSINK, J., CHRISTENSEN‐DALSGAARD, J., PATRICK, S.C. & CLUSELLA‐TRULLAS, S. (2020) Infrasonic hearing in birds: a review of audiometry and hypothesized structure–function relationships. Biological Reviews (Early view article). https://doi.org/10.1111/brv.12596

The long trip with the loggers

After over two years of planning and development, the Seabird Sound Infrasound loggers are off to the Southern Ocean. The loggers left France on 4th January, to join the Marion Dufresne in Réunion Island. After over a week at sea, sailing due South, they arrived on the Crozet Islands, in the French Sub-antarctic. Lying at 46 degrees South, Crozet is in one of the most remote, and windiest parts of the Earth. It is home to huge diversity of seabirds, and is particularly famous for its albatross and penguin colonies.

Our loggers will be deployed on Wandering Albatrosses, the largest albatross which can weigh up to 12kg and has a wing span of up to 3.5m. They can make foraging trips of up to 30 days and during their lifetime fly the equivalent distance to the moon and back 10 times.

Our logger, the ‘infrasound-sputnik’, has been designed as a low-cost mobile multidisciplinary measurement platform for geophysical monitoring. The platform is designed using digital Micro-electromechanical Systems (MEMS) sensors that are embedded on a Printed Circuit Board (PCB). The MEMS sensors on the PCB are a GPS, a three-component accelerometer, a barometric pressure sensor, an anemometer, and a differential pressure sensor. A programmable microcontroller unit controls the sampling frequency of the sensors. A weather and waterproof casing is used to protect the mobile platform. The casing is created with a stereolithography (SLA) Formlabs 3D printer, using durable raisin.

Thanks to low power consumption, the system can be powered by a battery or solar panel. After thorough calibration and comparison with reference sensors, it is found that the selected MEMS sensors are in good agreement when compared to high-fidelity equipment. Moreover, there is good consistency between the individual MEMS sensors.

So what does all of this mean? Our loggers are able to accurately measure infrasound and offer the opportunity to collect measurements in parts of the world that are inaccessible to traditional equipment. This is an example of how albatrosses can collect at-sea data on a huge range of parameter, crucial across scientific disciplines.

Perspectives on an interdisciplinary perspective

In May 2018, the eight of us and eleven experts from the fields of geophysics, animal hearing, movement ecology and seabird ecology gathered together in Liverpool to discuss whether animals, in particular seabirds, could use infrasound to navigate across the vast ocean. During the three-day workshop, funded by the Human Frontier Science Program (HFSP), we covered a wide range of topics from hydroacoustics to pigeon navigation and microbaroms to the magnetic sense of birds. The meeting was extremely productive, and we managed to identify some research priorities that will help link these disparate fields to better understand how birds hear and navigate. We departed with an agreement that we should formalize these ideas in paper form.

Workshop participants learning about infrasound and bird hearing from Olivier den Ouden and Jeff Zeyl, respectively.

A year and a half on, the “perspective” (this seemed the most appropriate term given the lack of empirical research on the topic) paper is taking shape. In the interim period, the SeabirdSound team have met several times and had lengthy, and sometimes intense, discussions about infrasound, bird navigation and hearing. Given the complexity of the topic and our diverse scientific backgrounds, it is understandable that it has taken some time to get a grasp of each other’s fields and sing from the same hymn sheet. Yet, we have agreed on several hypotheses which might explain how birds could use infrasound to navigate.

In November, in a bid to push the paper over the finish line, we decided to set aside some time to work on a complete draft. The global nature of this project – four research groups in three different continents – makes face-to-face meetings challenging. However, as we wanted to to reduce unnecessary travel time and our carbon footprints, we decided to try out a week-long “google hangout”. We were able to agree on a draft we are happy with, proving that it is possible to conduct truly global and collaborative research from our desks without the need for long-distance travel. We hope that in the new year the scientific community may benefit from our interdisciplinary contribution.

Dutch Bio-Acoustic conference

On Friday 11Oct, the Dutch Bio-Acoustic conference was organized. The gathering was held to share knowledge about the influence of acoustics on animal behavior. Scientist from VU Amsterdam, Leiden University, Wageningen University, Rijkswaterstaat, TNO, JASON, and VLIZ presented their results regarding noise pollution in the North Sea region (mostly underwater acoustics).

Olivier presented an overview of the SeabirdSound project under the scrutiny of the bio-acoustic experts. The talk was well received and opened fruitful discussions. This way, we like to thank RWS and the JOMOPANS project for organizing the conference, and we look forward to next year’s meeting!

Bio-logger

This week, I am precisely two years into the project! Besides this memorial milestone, we also finished one of the goals of our project! We finished the design of our logger for the upcoming fieldwork this January.

Last month I visited Dominique Fillipi, a well known and respected physicist who is specialized in developing Bio-loggers. Together with Dominique, I designed the “infrasound-sputnik”. This is the very first bio-logger, which besides tracking albatrosses, also can measure movement (acceleration), barometric pressure, differential pressure (infrasound), and wind speed/direction.

We worked on the hardware and software and did some first testing. We are all very excited and look forward to the outcome of the logger during the upcoming fieldwork.

Soon more updates on the logger!

Intense UK-France work trip (October-November 2018)

The Seabird Sound project is already in it’s second year and I’m still happy to be in this multidisciplinary team! (Have a look here if you’re getting lost with the many names in this text!). My role here is to develop and apply methods for movement analysis to contribute to a better understanding of seabird spatial behavior and how it is shaped by infrasound and meteorological conditions.

The seabird-ecology counterpart in the project is in Liverpool (Sam and Tommy) so we agreed that I would travel there to work with them. Since I had to make such a long trip from Fort Lauderdale, I decided to make the most of it, adding several destinations and working with as many people as possible.

This is a narrative of that month-and-a-half trip to Europe, by destination:

Chizé

The Centre d’Études Biologiques de Chizé (CEBC) is a CNRS lab is known for its research in marine mammals and seabirds, and for its scientific campaigns for data collection in faraway places like Kerguelen and Crozet islands. Sam, Tommy and I met in Chizé to discuss Tommy’s ideas for his paper on wind’s role on albatross behavior during foraging trips with Henri Weimerskirch. Henri has collected part of the data being analyzed and has worked with albatrosses for many years, so his feedback on Tommy’s findings was highly valuable. We also attended the outstanding PhD defense (viva) of Julien Collet, as Sam was a member of the jury, investigating strategies seabirds use to search and reach feeding areas. During this short but intense visit (2 days), I managed to squeeze in some time to finish a manuscript reviewing R packages and submitted it literally at the last minute: Not only was it the last day to submit the paper; we were also going to miss our train back to Paris if I didn’t finish on time. I made the quickest paper submission in my life so far (about 20-30 minutes) and I hope it will remain the quickest one.

Liverpool

This was the main destination of my trip. I was going to stay there for a bit more than two weeks so I had several tasks programmed for the journey.

The other postdocs of the project, Jeff and Ollie, joined Tommy and me at the University of Liverpool for the first week. We held meetings for just the four of us, to present our different topics of research to each other: introductions to our subjects, preliminary results and perspectives. I am very much familiar with Tommy’s research, as I play an active role in it. It was amazing to be able to learn from Ollie’s and Jeff’s own research.

ollie-pressure.jpeg
High and low pressure systems

At our request – or maybe just mine -, Ollie provided a great introductory talk to meteorology and its basic laws to help us understand how everything in meteorology is interconnected; thus also connected with infrasound. Jeff also gave an impressive introduction to hearing, and while it is hard to keep track of all the technical vocabulary, we enjoyed the presentation about auditory models and the anatomical comparison between terrestrial and aquatic bird species (read more about his research on this post). As I wanted to get more involved with the weather data analysis, Ollie shared a tutorial and gave me a script to download the ECMWF data, and we chatted about the links between atmospheric pressure and wind. It was all very helpful and I hope I can go visit him and Jelle at the Royal Netherlands Meteorological Institute soon!

During the second week, I focused more on working with Tommy to assess the effect of wind in albatross behavior during foraging trips via Hidden Markov modeling.

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Albatross track with inferred behaviors

There are at least two packages in R to implement Hidden Markov models (moveHMM and momentuHMM), making our tasks easier, but knowing how to parametrize the models and correctly interpret the results require understanding the intricacies of the methods as well as the ecology of the species. Together, a statistician and an ecologist, we’re trying to bring both components to the table for this piece of research—a manuscript should be ready in the next few months!

Working in Sam’s lab for a couple of weeks, I had the opportunity to participate in weekly lab meetings to discuss scientific articles and get to know a bit more about their research. I really felt like I was part of the lab during my stay, which is always a plus.

Avignon

After a long trip from Liverpool that took me the whole day, I arrived to Avignon for a workshop on SPDE (Stochastic Partial Differential Equations) modeling and INLA (Integrated Nested Laplace Approximation). I think that there is no need to say that this was a different scientific community than the seabird ecology department at the University of Liverpool.

inla
D. Allard, from RESSTE, introducing the SPDE workshop (picture taken by O. Gimenez)

The workshop was organized by the RESeau Statistiques pour données Spatio-TEmporelles (RESSTE) network and gathered a diverse public between applied (but quantitative) and theoretical researchers. Since I am considering using continuous time models for movement further in the HFSP project, I thought that learning an INLA approach would be handy for this. INLA can be a great solution to estimate parameters of complex models, and the organizers of the workshop provided a short introduction on how to express statistical models as SPDE that could be solved by INLA. Then, they showed the implementation of INLA in R (using R-INLA) with some examples of time series and spatial point processes. Some coauthors of the R-INLA and INLABRU packages were present and contributed to the seminars with their comments; that also made me realized that implementing INLA can be an incredibly difficult task for a model that has not been considered yet in the package. The seminars were complemented by the series of presentations from several participants on their research applying INLA.

Nantes

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View from my old flat in Nantes. I miss that.

After Avignon, I spent the weekend with some friends in Sète. Sète is a lovely small fishing city on the Mediterranean and one of the places I stayed in during my PhD. The weekend in Sète gave way to a three-week stay in Nantes. I did a previous postdoc at IFREMER in Nantes, and I was coming back this time to work on ‘old’ papers: one reviewing metrics to assess dyadic joint movement (now published in Movement Ecology) and one applying these metrics to several fleet movement data and learning about their collective behavior (almost ready to submit). My collaborators, which are not all from IFREMER, are quantitative researchers and founders of the trajectometry group Path Tool and analysIS (PathTIS). During my visit, we programmed meetings not only to discuss about the papers we needed to finish), but also to talk about my future projects to come again and collaborate on movement modeling papers.

Nantes was the last destination of this trip before heading back to Florida. All in all, I am very happy with all the work done and the scientific discussions. …And the wine, the food, the pubs, the funny conversations, the walks under the rain and the music. Thanks to everybody who welcomed me into their labs and cities, and the friends who hosted me. I had a blast and I hope to see you soon!

 

Fall Research Travels

It seems to be a good time to post a research update coming from the auditory physiology side of the project. I’m currently wrapping up a research trip to Europe, where I worked on multiple different components of the project with the other team members in the UK and Netherlands. Olivier and I also had a productive visit to a bird hearing expert earlier this week in Oldenburg, Germany.

I have been reviewing the scientific literature on low frequency hearing in birds, including the various experimental studies and hypothesized detection mechanisms. There are indeed many factors that can control the detection of low frequencies by birds. Sound vibrations move through the middle ear, inner ear, and auditory hair cells, ultimately becoming encoded into a neural signal at the end of the transmission line. At each of these levels, there are distinct structure-function relationships that will affect signal transmission. There is likely no single anatomical marker that will precisely reflect infrasonic hearing abilities, but the relevant anatomical parameters and how they might be expected to affect low frequency transmission is becoming clearer.

Multiple building blocks need to come together to pursue the big question, “do seabirds detect infrasound?”. One of these building blocks is a quantification of the large-scale patterns of auditory anatomy in seabirds. For this goal, I have been collecting microCT scans of seabird heads and skulls. In general, not a lot has been described on the auditory anatomy of seabirds.

The microCT images are quite cool to view and analyse. Below are microCT images of white-chinned petrel, Procellaria aequinoctialis (A). This species is commonly caught as bycatch from long-line fisheries vessels operating in South African waters, and that was my source for this particular specimen (thanks to folks at Capfish and BirdLife). You can even see a fish still in the throat and a bit of the hook apparatus on the lower right. Here are some additional images showing the reconstruction process for this technique. You can see clearly on this image the columella (middle ear bone of birds) and inner ear (B). After some analysis, the 3D models of specific components can be reconstructed (C,D).

One possible further application of the comparative microCT data is to use the 3D surface models to simulate acoustic transmission properties of the ear. This can be an option for animals for which direct hearing assessments are difficult, such as whales. The simulation models are then verified by direct vibrometric observation of middle ear. This technique might be a useful method for testing between the performance of different routes of acoustic stimulation. For example, the vibration transmission performance of the middle ear in tetrapod animals (including birds) generally declines towards low frequencies. Alternatively, sound at these very low frequencies might effectively couple to the whole body of the bird itself.

After some delay with getting permits  to collect seabird heads (partly due to restrictions related to the bird flu striking earlier in the year), we have the permissions we need and I hope to be examining many more species soon.4 in 1

SeabirdSound 2018 Workshop

From 14 till 17 May the first SeabirdSound workshop took place in Liverpool. The workshop focussed on infrasound and avian navigation and is part of the HFSP Project (investigating the role of infrasound in seabird navigation; it combines seabird ecology, physiology, infrasound soundscapes, and movement ecology in a comprehensive framework).

For the workshop, we brought together experts in all of these areas to share expertise and integrate ideas. In particular we were keen to discuss avian navigation in general with a focus on seabirds. By use of keynote presentations and engaging discussions, we developed an integrated framework around the use of infrasound in navigation and developed a begin for a review article around this subject. Follow the website for more news about this article.

We would like to thank all participants (alphabetic);

Simon Benhamou, Jakob Christensen-Dalsgaard, Annette Fayet, Jon Hagstrum, Christine Koppl, Emiel van Loon, Pascal Malkemper, Richard Phillips, Mark Prior, Pieter Smets and Yoshinari Yonehara.

And in particular Tommy Clay and Samantha Patrick for taking lead in organising!

 

EGU 2018 – Vienna

From 8 till 13 april the European Geosciences Union (EGU) organised the 2018 General Assembly in Vienna (Austria). During the assembly 4.776 oral, 11.128 poster, and 1.419 PICO presentations were given.

Jelle and Olivier represented the SeabirdSound team, both gave a poster presentation. Jelle presented his research about the Dutch Meteo-Tsunami of 29 May 2017. Olivier presented his studies on parameterising the CLEAN beamforming method on infrasound recordings.

Besides presenting, both participated many interesting presentations and short courses. It was an interesting week, good weather, good science and a good environment!

 

 

Master (MS) position in Movement Ecology at the University of Florida

We are seeking a motivated MS student to join our team in Florida, aiming at understanding how seabirds navigate and the role of infrasound in their movement. The MS thesis will follow one of two possible paths, requiring students with two distinct profiles: one in applied statistics/mathematics; and one in quantitative ecology. Applications are encouraged for both profiles, but only one student will be selected.

The Master’s program will consist of three semesters mainly dedicated to classwork during the first year and a second year exclusively dedicated to the Master’s thesis. This position will be completely supported for the two years (stipend + tuition) and the program is expected to start in fall 2018.

Classwork during the first two semesters will take place on the main UF campus in Gainesville. Research will be performed at Dr. Mathieu Basille’s lab, under the supervision of Dr. Basille and Dr. Rocio Joo. Dr. Basille’s lab is located at the University of Florida’s Fort Lauderdale Research and Education Center (FLREC), in Davie, Florida. Davie is a town within the large Miami metropolitan area in South Florida, just miles away from the Florida Everglades.

Full descriptionMasterAdvert-UF

!!please read the whole advertisement before sending your application!!

Please apply by sending an email including a cover letter describing your interest, experience and career goals, a CV, unofficial transcripts and GRE scores, and contact information for three references to Dr. Rocio Joo (rocio.joo@ufl.edu). Write “master application” as the email subject. Applications will be processed in the order they are received until April 15th or before if a suitable applicant is found.