Author: Clara Bird

How do we study the impact of whale watching?

Clara Bird, PhD Candidate, OSU Department of Fisheries, Wildlife, and Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

Since its start, the GEMM Lab has been interested in the effect of vessel disturbance on whales. From former student Florence’s masters project to Leila’s PhD work, this research has shown that gray whales on their foraging grounds have a behavioral response to vessel presence (Sullivan & Torres, 2018) and a physiological response to vessel noise (Lemos et al., 2022). Presently, our GRANITE project is continuing to investigate the effect of ambient noise on gray whales, with an emphasis on understanding how these effects might scale up to impact the population as a whole (Image 1).

To date, all this work has been focused on gray whales feeding off the coast of Oregon, but I’m excited to share that this is about to change! In just a few weeks, Leigh and I will be heading south for a pilot study looking at the effects of whale watching vessels on gray whale mom/calf pairs in the nursing lagoons of Baja California, Mexico.

Image 1. Infographic for the GRANITE project. Credit: Carrie Ekeroth

We are collaborating with a Fernanda Urrutia Osorio, a PhD candidate at Scripps Institute of Oceanography, to spend a week conducting fieldwork in one of the nursing lagoons. For this project we will be collecting drone footage of mom/calf pairs in both the presence and absence of whale watching vessels. Our goal is to see if we detect any differences in behavior when there are vessels around versus when there are not. Tourism regulations only allow the whale watching vessels to be on the water during specific hours, so we are hoping to use this regulated pattern of vessel presence and absence as a sort of experiment.

Image 2. A mom and calf pair.  NOAA/NMFS permit #21678.

The lagoons are a crucial place for mom/calf pairs, this is where calves nurse and grow before migration, and nursing is energetically costly for moms. So, it is important to study disturbance responses in this habitat since any change in behavior caused by vessels could affect both the calf’s energy intake and the mom’s energy expenditure. While this hasn’t yet been investigated for gray whales in the lagoons, similar studies have been carried out on other species in their nursing grounds.

Video 1. Footage of “likely nursing” behavior. NOAA/NMFS permit #21678.

We can use these past studies as blueprints for both data collection and processing. Disturbance studies such as these look for a wide variety of behavioral responses. These include (1) changes in activity budgets, meaning a change in the proportion of time spent in a behavior state, (2) changes in respiration rate, which would reflect a change in energy expenditure, (3) changes in path, which would indicate avoidance, (4) changes in inter-individual distance, and (5) changes in vocalizations. While it’s not necessarily possible to record all of these responses, a meta-analysis of research on the impact of whale watching vessels found that the most common responses were increases in the proportion of time spent travelling (a change in activity budget) and increased deviation in path, indicating an avoidance response (Senigaglia et al., 2016).

One of the key phrases in all these possible behavioral responses is “change in ___”. Without control data collected in the absence of whale watching vessels, it impossible to detect a difference. Some studies have conducted controlled exposures, using approaches with the research vessel as proxies for the whale watchers (Arranz et al., 2021; Sprogis et al., 2020), while others use the whale watching operators’ daily schedule and plan their data collection schedule around that (Sprogis et al., 2023). Just as ours will, all these studies collected data using drones to record whale behavior and made sure to collect footage before, during, and after exposure to the vessel(s).

One study focused on humpback mom/calf pairs found a decrease in the proportion of time spent resting and an increase in both respiration rate and swim speed during the exposure (Sprogis et al., 2020). Similarly, a study focused on short-finned pilot whale mom/calf pairs found a decrease in the mom’s resting time and the calf’s nursing time (Arranz et al., 2021). And, Sprogis et al.’s  study of Southern right whales found a decrease in resting behavior after the exposure, suggesting that the vessels’ affect lasted past their departure (Sprogis et al., 2023, Image 3). It is interesting that while these studies found changes in different response metrics, a common trend is that all these changes suggest an increase in energy expenditure caused by the disturbance.

However, it is important to note that these studies focused on short term responses. Long term impacts have not been thoroughly estimated yet. These studies provide many valuable insights, not only into the response of whales to whale watching, but also a look at the various methods used. As we prepare for our fieldwork, it’s useful to learn how other researchers have approached similar projects.

Image 3. Visual ethogram from Sprogis et al. 2023. This shows all the behaviors they identified from the footage.

I want to note that I don’t write this blog intending to condemn whale watching. I fully appreciate that offering the opportunity to view and interact with these incredible creatures is valuable. After all, it is one of the best parts of my job. But hopefully these disturbance studies can inform better regulations, such as minimum approach distances or maximum engine noise levels.

As these studies have done, our first step will be to establish an ethogram of behaviors (our list of defined behaviors that we will identify in the footage) using our pilot data. We can also record respiration and track line data. An additional response that I’m excited to add is the distance between the mom and her calf. Former GEMM Lab NSF REU intern Celest will be rejoining us to process the footage using the AI method she developed last summer (Image 4). As described in her blog, this method tracks a mom and calf pair across the video frames, and allows us to extract the distance between them. We look forward to adding this metric to the list and seeing what we can glean from the results.

Image 4. Example of a labelled frame from SLEAP, highlighting labels: rostrum, blowhole, dorsal, dorsal-knuckle, and tail. This labels are drawn to train the software to recognize the whales in unlabelled frames.

While we are just getting started, I am excited to see what we can learn about these whales and how best to study them. Stay tuned for updates from Baja!

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References

Arranz, P., Glarou, M., & Sprogis, K. R. (2021). Decreased resting and nursing in short-finned pilot whales when exposed to louder petrol engine noise of a hybrid whale-watch vessel. Scientific Reports, 11(1), 21195. https://doi.org/10.1038/s41598-021-00487-0

Lemos, L. S., Haxel, J. H., Olsen, A., Burnett, J. D., Smith, A., Chandler, T. E., Nieukirk, S. L., Larson, S. E., Hunt, K. E., & Torres, L. G. (2022). Effects of vessel traffic and ocean noise on gray whale stress hormones. Scientific Reports, 12(1), Article 1. https://doi.org/10.1038/s41598-022-14510-5

Senigaglia, V., Christiansen, F., Bejder, L., Gendron, D., Lundquist, D., Noren, D., Schaffar, A., Smith, J., Williams, R., Martinez, E., Stockin, K., & Lusseau, D. (2016). Meta-analyses of whale-watching impact studies: Comparisons of cetacean responses to disturbance. Marine Ecology Progress Series, 542, 251–263. https://doi.org/10.3354/meps11497

Sprogis, K. R., Holman, D., Arranz, P., & Christiansen, F. (2023). Effects of whale-watching activities on southern right whales in Encounter Bay, South Australia. Marine Policy, 150, 105525. https://doi.org/10.1016/j.marpol.2023.105525

Sprogis, K. R., Videsen, S., & Madsen, P. T. (2020). Vessel noise levels drive behavioural responses of humpback whales with implications for whale-watching. ELife, 9, e56760. https://doi.org/10.7554/eLife.56760

Sullivan, F. A., & Torres, L. G. (2018). Assessment of vessel disturbance to gray whales to inform sustainable ecotourism. Journal of Wildlife Management, 82(5), 896–905. https://doi.org/10.1002/jwmg.21462

Return of the whales: The GRANITE 2022 field season comes to a close

Clara Bird, PhD Candidate, OSU Department of Fisheries, Wildlife, and Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

It’s hard to believe that it’s already been four and half months since we started the field season (check out Lisa’s blog for a recap of where we began), but as of this weekend the GRANITE project’s 8th field season has officially ended! As the gray whales wrap up their foraging season and start heading south for the winter, it’s time for us to put our gear into storage, settle into a new academic year, and start processing the data we spent so much time collecting.

The field season can be quite an intense time (40 days equaling over 255 hours on the water!), so we often don’t take a moment to reflect until the end. But this season has been nothing short of remarkable. As you may remember from past blogs, the past couple years (2020-21) have been a bit concerning, with lower whale numbers than previously observed. Since many of us started working on the project during this time, most of us were expecting another similar season. But we were wrong in the best way. From the very first day, we saw more whales than in previous years and we identified whales from our catalog that we hadn’t seen in several years.

Image 1: Collage of photos from our field season.

We identified friends – old and new!

This season we had 224 sightings of 63 individual whales. Of those 63, 51 were whales from our catalog (meaning we have seen them in a previous season). Of these 51 known whales, we only saw 20 of them last year! This observation brings up interesting questions such as, where did most of these whales forage last year? Why did they return to this area this year? And, the classic end of season question, what’s going to happen next year?

We also identified 12 whales that were not in our catalog, making them new to the GEMM lab. Two of our new whales are extra exciting because they are not just new to us but new to the population; we saw two calves this year! We were fortunate enough to observe two mom-calf pairs in July. One pair was of a “new” mom in our catalog and her calf. We nicknamed this calf “Roly-poly” because when we found this mom-calf pair, we recorded some incredible drone footage of “roly-poly” continuously performing body rolls while their mom was feeding nearby (video 1). 

Video 1: “Roly-poly” body rolling while their mom headstands. NOAA/NMFS permit #21678.

The other pair includes a known GEMM lab whale, Luna, and her calf (currently nicknamed “Lunita”). We recently found “Lunita” feeding on their own in early October (Image 2), meaning that they are now independent from its mom (for more on mom-calf behavior check out Celest’s recent blog). We’ll definitely be on the lookout for Roly-Poly and Lunita next year!

Image 2: (left) drone image of Luna and Lunita together in July and (right) drone image of Lunita on their own in October.  NOAA/NMFS permit #21678.

We flew, we scooped, we collected heaps of data!

From our previous blogs you probably know that in addition to photo-ID images, our other two most important forms of data collection are drone flights (for body condition and behavior data) and fecal samples (for hormone analysis). And this season was a success for both! 

We conducted 124 flights over 49 individual whales. The star of these flights was a local favorite Scarlett who we flew over 18 different times. These repeat samples are crucial data for us because we use them to gain insight into how an individual’s body condition changes throughout the season. We also recorded loads of behavior data, collecting footage of different foraging tactics like headstanding, side-swimming, and surfacing feeding on porcelain crab larvae (video 2)!

Video 2: Two whales surface feeding on porcelain crab larvae. NOAA/NMFS permit #21678.

We also collected 61 fecal samples from 26 individual whales (Image 3). The stars of that dataset were Soléand Peak who tied with 7 samples each. These hard-earned samples provide invaluable insight into the physiology and stress levels of these individuals and are a crucial dataset for the project.

Image 3: Photos of fecal sample collection. Left – a very heavy sample, center: Lisa and Enrico after collecting the first fecal sample of the season, right: Clara and Lisa celebrating a good fecal sample collection.

On top of all that amazing data collection we also collected acoustic data with our hydrophones, prey data from net tows, and biologging data from our tagging efforts. Our hydrophones were in the water all summer recording the sounds that the whales are exposed to, and they were successfully recovered just a few weeks ago (Image 4)! We also conducted 69 net tows to sample the prey near where the whales were feeding and identify which prey the whales might be eating (Image 5). Lastly, we had two very successful tagging weeks during which we deployed (and recovered!) a total of 9 tags, which collected over 30 hours of data (Image 6; check out Kate’s blog for more on that).

Image 4 – Photos from hydrophone recovery.
Image 5: Photos from zooplankton sampling.
Image 6: Collage of photos from our two tagging efforts this season.

Final thoughts

All in all, it’s been an incredible season. We’ve seen the return of old friends, collected lots of awesome data, and had some record-breaking days (28 whales in one day!). As we look toward the analysis phase of the year, we’re excited to dig into our eight-year dataset and work to understand what might explain the increase in whales this year.

To end on a personal note, looking through photos to put in this blog was the loveliest trip down memory lane (even though it only ended a few days ago) – I am so honored and proud to be a part of this team. The work we do is hard; we spend long hours on a small boat together and it can be a bit grueling at times. But, when I think back on this season, my first thoughts are not of the times I felt exhausted or grumpy, but of all the joy we felt together. From the incredible whale encounters to the revitalizing snacks to the off-key sing alongs, there is no other team I would rather do this work with, and I so look forward to seeing what next season brings. Stay tuned for more updates from team GRANITE!

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Putting Fitbits on whales: How tag data allows for estimating calories burned by foraging PCFG gray whales

By: Kate Colson, MSc Student, University of British Columbia, Institute for the Oceans and Fisheries, Marine Mammal Research Unit

Hello! My name is Kate Colson and I am a master’s student at the University of British Columbia, co-supervised by Dr. Andrew Trites of the Marine Mammal Research Unit and Dr. Leigh Torres of the GEMM Lab. As part of my thesis work, I have had the opportunity to spend the summer field season with Leigh and the GEMM Lab team. 

For my master’s I am studying the foraging energetics of Pacific Coast Feeding Group (PCFG) gray whales as part of the much larger Gray whale Response to Ambient Noise Informed by Technology and Ecology (GRANITE) project. Quantifying the energy expenditure of PCFG gray whales during foraging can help establish a baseline for how disturbance impacts the ability of this unique population to meet their energy needs. Additionally, determining how many calories are burned during different PCFG foraging behaviors might help explain why some gray whales are in better body condition than others.

To understand how much energy different PCFG foraging behaviors cost, I am using data from suction cup tags we have temporarily applied on PCFG gray whales (Figure 1). You can read more about the why the GEMM Lab started using these tags in an earlier blog here. What I want to talk about in this blog is how exactly we can use this tag data to estimate energy expenditure of PCFG gray whales. 

Figure 1. The famous “Scarlett” with a suction cup tag just attached using a carbon fiber pole (seen on far right). This minimally invasive tag has many data sensors, all of which sample at high frequencies, that can allow for an estimation of energy expenditure for different gray whale behaviors. Source: GEMM Lab; National Marine Fisheries Service (NMFS) permit no. 21678 

The suction cups tags used in this project have many data sensors that are useful for describing the movement of the tagged whale including accelerometers, magnetometers, gyroscopes, and pressure sensors, and all are sampling at high frequencies. For example, the accelerometer is taking 400 measurements per second! The accelerometer, magnetometer, and gyroscope take measurements in 3 dimensions along the X, Y, and Z-axes. The whale’s movement around the X-axis indicates roll (if the whale is swimming on its side), while movement around the Y-axis indicates pitch (if the whales head is oriented towards the surface or the sea floor). Changes in the whale’s movement around the Z-axis indicates if the whale is changing its swimming direction. Together, all of these sensors can describe the dive profile, body orientation, fluking behavior, and fine-scale body movements of the animal down to the second (Figure 2). This allows for the behavior of the tagged whale to be specifically described for the entirety of the tag deployment. 

Figure 2. An example of what the tag sensor data looks like. The top panels show the depth of the animal and can be used to determine the diving behavior of the whale. The middle panels show the body roll of the whale (the X axis) —a roll value close to 0 means the whale is swimming “normally” with no rotation to either side, while a higher roll value means the whale is positioned on its side. The bottom panels show the fluking behavior of the animal: each spike is the whale using its tail to propel itself through the water, with higher spikes indicating a stronger fluke stroke. Source: GEMM Lab, NMFS permit no. 21678

Although these suction cup tags are a great advancement in collecting fine-scale data, they do not have a sensor that actually measures the whale’s metabolism, or rate of calories burned by the whale. Thus, to use this fine-scale tag data as an estimate for energy expenditure, a summary metric must be calculated from the data and used as a proxy. The most common metric found in the literature is Overall Dynamic Body Acceleration (ODBA) and many papers have been published discussing the pros and cons of using ODBA as a proxy for energy expenditure (Brown et al., 2013; Gleiss et al., 2011; Halsey, 2017; Halsey et al., 2011; Wilson et al., 2020). The theory behind ODBA is that because an animal’s metabolic rate is primarily comprised of movement costs, then measuring the acceleration of the body is an effective way of determining energy expenditure. This theory might seem very abstract, but if you have ever worn a Fitbit or similar fitness tracking device to estimate how many calories you’ve burned during a workout, the same principle applies. Those fitness devices use accelerometers and other sensors, to measure the movement of your limbs and produce estimates of energy used. 

So now that we’ve established that the goal of my research is to essentially use these suction cup tags as Fitbits for PCFG gray whales, let’s look at how accelerometry data has been used to detect foraging behavior in large whales so far. Many accelerometry tagging studies have used rorquals as a focal species (see Shadwick et al. (2019) for a review). Well-known rorqual species include humpback, fin, and blue whales. These species forage by using lunges to bulk feed on dense prey patches in the water column. Foraging lunges are indicated by isolated periods of high acceleration that are easily detectable in the tag data (Figure 3; Cade et al., 2016; Izadi et al., 2022). 

Figure 3. Top image: A foraging blue whale performing a surface lunge (Photo credit: GEMM Lab). Note the dense aggregation of krill in the whale’s mouth. Bottom image: The signature acceleration signal for lunge feeding (adapted from Izadi et al., 2022). Each color represents one of the 3D axes of whale movement. The discrete periods of high acceleration represent lunges. 

However, gray whales feed very differently from rorquals. Gray whales primarily suction feed on the benthos, using their head to dig into the sediment and filter prey out of the mud using their baleen. Yet,  PCFG gray whales often perform many other foraging behaviors such as headstanding and side-swimming (Torres et al., 2018). Additionally, PCFG gray whales tend to feed in water depths that are often shallower than their body length. This shallow depth makes it difficult to isolate signals of foraging in the accelerometry data from random variation in the data and separate the tag data into periods of foraging behaviors (Figure 4).

Figure 4. Top image: A foraging PCFG gray whale rolls on its side to feed on mysid prey. Bottom image: The graph shows the accelerometry data from our suction cup tags that can be used to calculate Overall Dynamic Body Acceleration (ODBA) as a way to estimate energy expenditure. Each color represents a different axis in the 3D motion of the whale. The X-axis is the horizontal axis shows forward and backward movement of the whale, the Y-axis shows the side-to-side movement of the whale, and the Z-axis shows the up-down motion of the whale. Note how there are no clear periods of high acceleration in all 3 axes simultaneously to indicate different foraging behaviors like is apparent during lunges of rorqual whales. However, there is a pattern showing that when acceleration in the Z-axis (blue line) is positive, the X- and Y-axes (red and green lines) are negative. Source: GEMM Lab; NMSF permit no. 21678

But there is still hope! Thanks to the GEMM Lab’s previous work describing the foraging behavior of the PCFG sub-group using drone footage, and the video footage available from the suction cup tags deployed on PCFG gray whales, the body orientation calculated from the tag data can be a useful indication of foraging. Specifically, high body roll is apparent in many foraging behaviors known to be used by the PCFG, and when the tag data indicates that the PCFG gray whale is rolled onto its sides, lots of sediment (and sometimes even swarms of mysid prey) is seen in the tag video footage. Therefore, I am busy isolating these high roll events in the collected tag data to identify specific foraging events. 

My next steps after isolating all the roll events will be to use other variables such as duration of the roll event and body pitch (i.e., if the whales head is angled down), to define different foraging behaviors present in the tag data. Then, I will use the accelerometry data to quantify the energetic cost of performing these behaviors, perhaps using ODBA. Hopefully when I visit the GEMM Lab again next summer, I will be ready to share which foraging behavior leads to PCFG gray whales burning the most calories!

References: 

Brown, D. D., Kays, R., Wikelski, M., Wilson, R., & Klimley, A. P. (2013). Observing the unwatchable through acceleration logging of animal behavior. Animal Biotelemetry, 1(1), 1–16. https://doi.org/10.1186/2050-3385-1-20

Cade, D. E., Friedlaender, A. S., Calambokidis, J., & Goldbogen, J. A. (2016). Kinematic diversity in rorqual whale feeding mechanisms. Current Biology, 26(19), 2617–2624. https://doi.org/10.1016/j.cub.2016.07.037

Duley, P. n.d. Fin whales feeding [photograph]. NOAA Northeast Fisheries Science Center Photo Gallery. https://apps-nefsc.fisheries.noaa.gov/rcb/photogallery/finback-whales.html

Gleiss, A. C., Wilson, R. P., & Shepard, E. L. C. (2011). Making overall dynamic body acceleration work: On the theory of acceleration as a proxy for energy expenditure. Methods in Ecology and Evolution, 2(1), 23–33. https://doi.org/10.1111/j.2041-210X.2010.00057.x

Halsey, L. G. (2017). Relationships grow with time: A note of caution about energy expenditure-proxy correlations, focussing on accelerometry as an example. Functional Ecology, 31(6), 1176–1183. https://doi.org/10.1111/1365-2435.12822

Halsey, L. G., Shepard, E. L. C., & Wilson, R. P. (2011). Assessing the development and application of the accelerometry technique for estimating energy expenditure. Comparative Biochemistry and Physiology – A Molecular and Integrative Physiology, 158(3), 305–314. https://doi.org/10.1016/j.cbpa.2010.09.002

Izadi, S., Aguilar de Soto, N., Constantine, R., & Johnson, M. (2022). Feeding tactics of resident Bryde’s whales in New Zealand. Marine Mammal Science, 1–14. https://doi.org/10.1111/mms.12918

Shadwick, R. E., Potvin, J., & Goldbogen, J. A. (2019). Lunge feeding in rorqual whales. Physiology, 34, 409–418. https://doi.org/10.1152/physiol.00010.2019

Torres, L. G., Nieukirk, S. L., Lemos, L., & Chandler, T. E. (2018). Drone up! Quantifying whale behavior from a new perspective improves observational capacity. Frontiers in Marine Science, 5, 1–14. https://doi.org/10.3389/fmars.2018.00319

Wilson, R. P., Börger, L., Holton, M. D., Scantlebury, D. M., Gómez-Laich, A., Quintana, F., Rosell, F., Graf, P. M., Williams, H., Gunner, R., Hopkins, L., Marks, N., Geraldi, N. R., Duarte, C. M., Scott, R., Strano, M. S., Robotka, H., Eizaguirre, C., Fahlman, A., & Shepard, E. L. C. (2020). Estimates for energy expenditure in free-living animals using acceleration proxies: A reappraisal. Journal of Animal Ecology, 89(1), 161–172. https://doi.org/10.1111/1365-2656.13040

Do you lose SLEAP over video analysis of gray whale behavior? Not us in the GEMM Lab! 

Celest Sorrentino, University of California, Santa Barbara, Department of Ecological, Evolution, and Marine Biology, GEMM Lab NSF REU intern

Are you thinking “Did anyone proofread this blog beforehand? Don’t they know how to spell SLEEP?”  I completely understand this concern, but not to fear: the spelling of SLEAP is intentional! We’ll address that clickbait in just a moment. 

My name is Celest Sorrentino, a first-generation Latina undergrad who leaped at the opportunity to depart from the beaches of Santa Barbara, California to misty Newport, Oregon to learn and grow as a scientist under the influential guidance of Clara Bird, Dr. Leigh Torres and the powerhouse otherwise known as the GEMM lab. As a recent NSF REU (Research Experience for Undergraduates) intern in the GEMM Lab at Oregon State University, I am thrilled to have the chance to finally let you in on the project Clara, Leigh and I have been working on all summer. Ready for this?

Our project uses a deep-learning platform called SLEAP A.I. ( https://sleap.ai/) that can predict and track multiple animals in video to track gray whale mother calf pairs in drone footage. We also took this project a step further and explored how the distance between a gray whale mother and her calf, a proxy for calf independence, varied throughout the season and by different calf characteristics. 

In this story, we’ve got a little bit for everyone: the dynamic duo of computer vision and machine learning for my data scientist friends, and ecological inquest for my cetacean researcher friends. 

About the Author

Before we begin, I’d like to share that I am not a data scientist. I’ve only ever taken one coding class. I also do not have years of gray whale expertise under my belt (not yet at least!). I’m entering my 5th year at University of California, Santa Barbara as a double major in Ecology and Evolution (BS) as well as Italian Studies (BA). I am sharing this information to convey the feasibility of learning how to use machine-learning as a solution to streamline the laborious task of video analysis, which would permit more time towards answering your own ecological question, as we did here.

Essential Background

Hundreds of Hours of Drone footage

Since 2016, the GEMM Lab has been collecting drone footage of gray whales off the Oregon Coast to observe gray whale behavior in more detail (Torres et al. 2018). Drones have been shown to increase observational time of gray whales by a three-fold (Torres et al. 2018), including the opportunity to revisit the video with fresh eyes at any time one pleases. The GEMM Lab has flow over 500 flights in the past 6 years, including limited footage of gray whale mother-calf pairs. Little is known about gray whale mother-calf dynamics and even less about factors that influence calf development. As we cannot interview hundreds of gray-whale mother-calf pairs to develop a baseline for this information, we explore potential proxies for calf development instead (similar to how developmental benchmarks are used for human growth). 

Distance and Development

During our own life journey, each of us became less and less dependent on our parents to survive on our own. Formulating our first words so that we can talk for ourselves, cracking an egg for our parents so that we can one day cook for ourselves, or even letting go of their hand when crossing the street. For humans, we spend many years with our kin preparing for these moments, but gray whale mother-calf pairs only have a few months after birth until they separate. Gray whale calves are born on their wintering grounds in Baja California, Mexico (around February), migrate north with their mothers to the foraging grounds, and are then weaned during the foraging season (we think around August). This short time with their mother means that they have to become independent pretty quickly (about 6 months!).

Distance between mother and calf can be considered a measure of independence because we would expect increased distance between the pair as calf independence increases. In a study by Nielson et al (2019), distance between Southern Right Whale mother-calf pairs was found to increase as the calf grew, indicating that it can serve as a good proxy for independence. The moment a mother-calf pair separates has not been documented, but the GEMM lab has footage of calves during the foraging season pre-weaning that can be used to investigate this process.  However, video analysis is no easy feat: video analysis can range from post-processing, diligent evaluation, and video documentation (Torres et al. 2018). Although the use of UAS has become a popular method for many researchers, the extensive time required for video analysis is a limitation. As mentioned in Clara’s blog, the choice to pursue different avenues to streamline this process, such as automation through machine learning, is highly dependent on the purpose and the kind of questions a project intends to answer.

SLEAP A.I.

 In a world where modern technology is constantly evolving to cater towards making everyday tasks easier, machine learning leads the charge with its ability for a machine to perform human tasks. Deep learning is a subset of machine learning in which the model learns and adapts the ability to perform a task given a dataset. SLEAP (Social LEAP Estimation of Animal Poses) A.I. is an open-source deep-learning framework created to be able to track multiple subjects, specifically animals, throughout a variety of environmental conditions and social dynamics. In previous cases, SLEAP has tracked animals with distinct morphologies and conditions such as mice interactions, fruit flies engaging in courtship, and bee behavior in a petri dish (Pereira 2020). While these studies show that SLEAP could help make video analysis more efficient, these experiments were all conducted on small animals and in controlled environments. However, large megafauna, such as gray whales, cannot be cultivated and observed in a controlled Petri dish. Could SLEAP learn and adapt to predict and track gray whales in an uncontrolled environment, where conditions are never the same (ocean visibility, sunlight, obstructions)? 

Methods

In order to establish a model within SLEAP, we split our mother-calf drone video dataset into training (n=9) and unseen/testing (n=3) videos. Training involves teaching the model to recognize gray whales, and necessitated me to label every four frames using the following labels (anatomical features): rostrum, blowhole, dorsal, dorsal-knuckle, and tail (Fig. 1). Once SLEAP was trained and able to successfully detect gray whales, we ran the model on unseen video. The purpose of using unseen video was to evaluate whether the model could adapt and perform on video it had never seen before, eliminating the need for a labeler to retrain it. 

We then extracted the pixel coordinates for the mom and calf, calculated the distance between their respective dorsal knuckles, and converted the distance to meters using photogrammetry (see KC’s blog  for a great explanation of these methods).  The distance between each pair was then summarized on a daily scale as the average distance and the standard deviation. Standard deviation was explored to understand how variable the distance between mother-calf pair was throughout the day. We then looked at how distance and the standard deviation of distance varied by day of year, calf Total Length (TL), and calf Body Area Index (BAI; a measure of body condition). We hypothesized that these three metrics may be drivers of calf independence (i.e., as the calf gets longer or fatter it becomes more independent from its mother).  

Fig 1. Example of a labelled frame from SLEAP, highlighting labels: rostrum, blowhole, dorsal, dorsal-knuckle, and tail. 

Results

SLEAP A.I. was able to successfully detect and track gray whale mother-calf pairs across all videos (that’s a total of 1318 frames!). When evaluating how the average distance changed across Day of Year, calf Total length, and calf BAI, the plots did not demonstrate the positive relationship we anticipated (Fig 2A). However, when evaluating the standard deviation of distance across Day of Year, calf Total Length, and calf BAI, we did notice that there does appear to be an increase in variability of distance with an increase in Day of Year and calf Total length (Fig 2B)

Fig 2A: Relationship between average distance(m) between each mother and calf (colors represent different named calves) relative to Day of Year, Total length of calf, and BAI of calf. 
Fig 2B: Relationship between standard deviation of  distance(m) between each mother and calf (colors represent different named calves) relative to Day of Year, Total length of calf, and BAI of calf.

Concluding thoughts

These results are monumental! We demonstrated the feasibility to use AI to create a model that can track gray whale pairs in drone footage, which is a fantastic tool that can be applied to updated datasets in the future. As more footage of gray whale mother-calf pairs are collected, this video can be quickly uploaded to SLEAP for model evaluation, predictions can be exported, and results subsequently included in the distance analysis to update our plots and increase our understanding. Our data currently provide a preliminary understanding of how the distance between mother-calf pairs changes with Day of Year, Total length, and BAI, but we are now able to continue updating our dataset as we collect more drone footage. 

I suppose you can say I did mislead you a bit with my title, as I have lost some SLEEP recently. But, not over video analysis per say but rather in the form of inspiration. Inspiration toward expanding my understanding of machine learning so that it can be applied toward answering pressing ecological questions. This project has only propelled me to dig my heels in and investigate further the potential of machine learning to analyze dense datasets for huge knowledge gains.

Fig 3A: Snapshot of Celest working in SLEAP GUI.

Acknowledgements

This project was made possible in partnership by the continuous support by Clara Bird, Dr. Leigh Torres, KC Bierlich, and the entire GEMM Lab!

References

Nielsen, M., Sprogis, K., Bejder, L., Madsen, P., & Christiansen, F. (2019). Behavioural development in southern right whale calves. Marine Ecology Progress Series, 629, 219–234. https://doi.org/10.3354/meps13125

Pereira, Talmo D., Nathaniel Tabris, Junyu Li, Shruthi Ravindranath, Eleni S. Papadoyannis, Z. Yan Wang, David M. Turner, et al. “SLEAP: Multi-Animal Pose Tracking.” Preprint. Animal Behavior and Cognition, September 2, 2020. https://doi.org/10.1101/2020.08.31.276246.

Torres, Nieukirk, S. L., Lemos, L., & Chandler, T. E. (2018). Drone Up! Quantifying Whale Behavior From a New Perspective Improves Observational Capacity. Frontiers in Marine Science, 5. https://doi.org/10.3389/fmars.2018.00319

Grad school growing pains

Clara Bird, PhD Candidate, OSU Department of Fisheries, Wildlife, and Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

“What if I’m wrong? What if I make a mistake?” When I began my career after completing my undergraduate degree, these questions echoed constantly in my head as the stakes were raised and my work was taken more seriously. Of course, this anxiety was not new. As a student, my worst fear had been poor performance in class. Post-undergrad, I was facing the possibility of making a mistake that could impact larger research projects and publications. 

Gaining greater responsibility and consequences is a fact of life and an intrinsic part of growing up. As I wrap up my third year of graduate school, I’ve been reflecting on how learning to take on this responsibility as a scientist has been a crucial part of my journey thus far.  

A scientist’s job is to ask, and try to answer, questions that no one knows the answer to – which is both terrifying and exciting. It feels a bit like realizing that grown-ups don’t have all the answers as a kid. Becoming comfortable with the fact that my work often involves making decisions that no one definitively can say are wrong or right has been one of my biggest challenges of grad school. The important thing to remember, I’ve learned, is that I’m not making wild guesses – I’m being trained to make the best, most informed decisions possible. And, hopefully, with more experience will come greater confidence. 

Through grad school I have learned to take on this responsibility both in the field and the lab, although each brings different experiences. In the field, the stakes can feel higher because the decisions we make affect not just the quality of the data, but the safety of the team (which is always the top priority). I felt this most acutely throughout my first summer as a drone pilot. As a pilot, I am responsible for the safety of the team, the drone, and the quality of the data. As a new pilot, I intensely felt this pressure and would come home feeling more exhausted than usual. Now, in my second field season in this role, I’ve become more comfortable and am slowly building confidence in my abilities as I gain more and more experience. 

Video 1 – Two gray whales foraging together off Newport, Oregon, USA. I recorded this footage during my first season as a pilot – a flight I’ll never forget! NOAA/NMFS permit #21678.

I have also had a similar experience in the lab. Once it’s time to work on the analysis of a project, I choose how to clean, analyze, and interpret the data. As a young scientist, every step of the process involves learning new skills and making decisions that I don’t feel entirely qualified to make.  When I started analysis for my first PhD chapter, I felt overwhelmed by deciding how to standardize my data, what kind of analysis to perform, and what indices to calculate. And, since it’s my first chapter, I felt further overwhelmed by the worry that any decision I made would become a later regret in a future part of my PhD. 

Recently, the most daunting decision has been how to standardize my data. For my first chapter, I am investigating individual specialization of gray whale foraging behavior. The results of this question are not only important for conservation, but for my subsequent work (check out these previous blogs from January 2021and April 2022 for more on this research question). While there is a wealth of literature to draw analysis inspiration from, most of these studies use discrete prey capture data, while I am working with continuous behavior data. So, to make my data points comparable to one another, I need to standardize the behavior observation time of each drone flight to account for the potential bias introduced by recording one individual for more time than another. After experiencing an internal roller coaster of having an idea, thinking it through, deciding it was terrible and restarting the cycle, I was reminded that turning to lab mates and collaborators is the best way to work through a problem.

Image 1 – Comic from phdcomics.com, source: https://phdcomics.com/comics/archive.php?comicid=2008

So, I had as many conversations as I could with my advisor, committee members, and peers. My thinking clarified with every conversation, and I gained confidence in the justification behind my decision. I cannot fully express the comfort that comes from hearing a trusted advisor say, “that makes ecological sense to me”. These conversations have also helped me remember that I am not alone in my worry and that I am not failing because I have these doubts.  While I may never be 100% convinced that I’ve made the right decision, I feel much better knowing that I’ve talked it through with the brilliant group of scientists around me. And as I enter an analysis-intensive phase of my PhD, I am extremely grateful to have this community around to challenge, advise, and support me. 

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What drives individual specialization?

Clara Bird, PhD Student, OSU Department of Fisheries, Wildlife, and Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

When I wrote my first blog on individual specialization well over a year ago, I just skimmed the surface of the literature on this topic and only started to recognize the importance of studying individual specialization. The question, “is there individual specialization in the PCFG of gray whales?” is the focus of my first thesis chapter and the results will affect all my subsequent work. Therefore, the literature and concepts of individual specialization are a focus of my literature review and studies.

In my previous blog I focused on common characteristics of individuals that are similarly specialized as an underlying driver of individual specialization. While these characteristics (often attributable to age, sex, or physical traits) are important to consider, I’ve learned that the list of drivers of individual specialization is long and that many variables are dynamic. Of all the drivers I’ve learned about, competition is among the most common.

Competition is a major driver of individual specialization, and a common driver of competition is resource availability. When resource availability decreases, whether caused by increasing population density or changing environmental conditions, competition for that resource increases. As competition increases, individuals have a choice. They can choose to engage in competition, either by racing, fighting, or sharing [1], which can be costly, or they can diffuse the competition by focusing on a different resource.  This second approach would be considered niche partitioning in the prey dimension. Niche partitioning is a way for individuals to share ecological space by using different resources. Essentially, individuals can share habitat without having to engage in direct competition by pursuing different prey types [2]. 

This switch to different prey types can change the degree of individual specialization present in the population (Figure 1). But the direction of the change is not constant. If all individuals were pursuing the same prey type under low competition conditions but then switched to different alternate prey types under high competition, then individual specialization would increase (Figure 1a). This direction has been observed across a range of species including sharks [3], otters [4]–[7], dolphins [8], [9], stickleback fish [10], [11], largemouth bass [12], banded mongoose [13], fur seals [14], and baleen whales [15].

However, if individuals were pursuing different prey types under low competition conditions (maybe because of underlying differences such as age or sex) but then switched to the same alternate prey types under high competition, diet overlap would increase, and individual specialization would decrease (Figure 1b). Furthermore, an individual might not switch to an entirely new prey type but instead add prey items to its diet [16]. This diet expansion under competition would also decrease individual specialization. Fewer studies have reported this direction but it’s been found in the common bumblebee [17] and in several neotropical vertebrate species [18], [19].

Figure `1. Figure 3 from Araújo et al. 2011 [20]. Illustration of how ecological mechanisms may affect the degree of individual specialization. Arrows linking resources to individual consumers indicate resource consumption (relative thickness indicates proportional contribution). 
Horizontal arrows indicate the sign (positive or negative) of the effect on the degree of individual specialization. (a) Consumers share the same preferred resource (dark gray tangle) but have different alternative resources (white and light gray triangles). As the preferred resource becomes scarce, consumers switch to different alternatives, increasing the degree of individual specialization. (b) Alternatively, consumers have distinct preferred resources, so that as resources become scarce, individuals converge to the alternative resource (dark gray triangle), reducing diet variation.

Interestingly, its hypothesized that individual specialization driven by competition is one of the factors that facilitates the formation and existence of stable groups [21]. For example, a study on resident female dolphins in Sarasota Bay, FL, USA found that females with high spatial overlap used distinct foraging specializations [8](Figure 2). This study illustrates how partitioning prey enabled spatial and social coexistence. A study on banded mongooses reached a similar conclusion [13]. They found that specialization was highest in the biggest groups (with the most competition) and not explained by sex, age, or other inherent differences. They hypothesized that specialization increasing with competition reduced conflict and allowed the groups to remain stable. This study also highlighted the role of learning to determine an individual’s specialization.

Figure 2. A bottlenose dolphin.
Source: https://sarasotadolphin.org

Learning drives the distribution of knowledge throughout a population, which can lead to either specialization or generalization. ‘One-to-one’ learning, where one individual learns from one demonstrator, tends to promote individual specialization [21]. This form of transmission drives specialization because the individuals who learn the specialization tend to then carry on using, and eventually teaching, that specialization [6]. A common example of ‘one-to-one’ learning is vertical transmission from parent to offspring. It has been shown to transmit specializations in dolphins [22] and otters [6]. ‘One-to-one’ learning can occur outside of parent-offspring pairs; non-parent-offspring ‘one-to-one’ learning has been shown to drive specialization in banded mongooses [13](Figure 3).

However, other forms of social learning can promote more generalized foraging strategies. ‘Many-to-one’ or ‘one-to-many’ learning  can reduce the presence of specialization in species [13], [21] as can the presence of conformity in a group [23], [24].

Figure 3. A group of banded mongooses.
Source: http://socialisresearch.org/about-the-banded-mongoose-project/

The multiple drivers of specialization and their dynamic quality means that it is important to contextualize specialization. For example, a study on four species of neotropical frogs found varying degrees of specialization across multiple populations of each species [18]. The degree of specialization was dependent on a variety of drivers including predation and both intra- and inter-specific competition. Notably, the direction of the relationship between degree of specialization and each driver was species specific. This study highlights that one species may not always be more specialized than another, but that a populations’ specialization is context dependent.

Therefore, it is important to not only be aware of the degree of specialization present in a population, but to also understand its dynamics and drivers. These relationships can then be used to understand how, and why, a population may react to competition from other species, predators, and changes in resource availability [20].  A population’s specialization can also affect the specialization of other populations and community dynamics [25], therefore, it’s important to consider and study individual specialization on both the population and community level. I am excited to start using our incredible six-year dataset to start investigating these questions for PCFG gray whales, so stay tuned for results!

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References

[1]       M. Taborsky, M. A. Cant, and J. Komdeur, The Evolution of Social Behaviour. Cambridge: Cambridge University Press, 2021. doi: 10.1017/9780511894794.

[2]       E. R. Pianka, “Niche Overlap and Diffuse Competition,” vol. 71, no. 5, pp. 2141–2145, 1974.

[3]       P. Matich et al., “Ecological niche partitioning within a large predator guild in a nutrient-limited estuary,” Limnol. Oceanogr., vol. 62, no. 3, pp. 934–953, 2017, doi: https://doi.org/10.1002/lno.10477.

[4]       S. D. Newsome et al., “The interaction of intraspecific competition and habitat on individual diet specialization: a near range-wide examination of sea otters,” Oecologia, vol. 178, no. 1, pp. 45–59, May 2015, doi: 10.1007/s00442-015-3223-8.

[5]       M. T. Tinker, G. Bentall, and J. A. Estes, “Food limitation leads to behavioral diversification and dietary specialization in sea otters,” Proc. Natl. Acad. Sci., vol. 105, no. 2, pp. 560–565, Jan. 2008, doi: 10.1073/pnas.0709263105.

[6]       M. T. Tinker, M. Mangel, and J. A. Estes, “Learning to be different: acquired skills, social learning, frequency dependence, and environmental variation can cause behaviourally mediated foraging specializations,” Evol. Ecol. Res., vol. 11, pp. 841–869, 2009.

[7]       M. T. Tinker et al., “Structure and mechanism of diet specialisation: testing models of individual variation in resource use with sea otters,” Ecol. Lett., vol. 15, no. 5, pp. 475–483, 2012, doi: 10.1111/j.1461-0248.2012.01760.x.

[8]       S. Rossman et al., “Foraging habits in a generalist predator: Sex and age influence habitat selection and resource use among bottlenose dolphins (Tursiops truncatus),” Mar. Mammal Sci., vol. 31, no. 1, pp. 155–168, 2015, doi: https://doi.org/10.1111/mms.12143.

[9]       L. G. Torres, “A kaleidoscope of mammal , bird and fish : habitat use patterns of top predators and their prey in Florida Bay,” vol. 375, pp. 289–304, 2009, doi: 10.3354/meps07743.

[10]     M. S. Araújo et al., “Network Analysis Reveals Contrasting Effects of Intraspecific Competition on Individual Vs. Population Diets,” Ecology, vol. 89, no. 7, pp. 1981–1993, 2008, doi: 10.1890/07-0630.1.

[11]     R. Svanbäck and D. I. Bolnick, “Intraspecific competition drives increased resource use diversity within a natural population,” Proc. R. Soc. B Biol. Sci., vol. 274, no. 1611, pp. 839–844, Mar. 2007, doi: 10.1098/rspb.2006.0198.

[12]     D. E. Schindler, J. R. Hodgson, and J. F. Kitchell, “Density-dependent changes in individual foraging specialization of largemouth bass,” Oecologia, vol. 110, no. 4, pp. 592–600, May 1997, doi: 10.1007/s004420050200.

[13]     C. E. Sheppard et al., “Intragroup competition predicts individual foraging specialisation in a group-living mammal,” Ecol. Lett., vol. 21, no. 5, pp. 665–673, 2018, doi: 10.1111/ele.12933.

[14]     L. Kernaléguen, J. P. Y. Arnould, C. Guinet, and Y. Cherel, “Determinants of individual foraging specialization in large marine vertebrates, the Antarctic and subantarctic fur seals,” J. Anim. Ecol., vol. 84, no. 4, pp. 1081–1091, 2015, doi: 10.1111/1365-2656.12347.

[15]     E. M. Keen and K. M. Qualls, “Respiratory behaviors in sympatric rorqual whales: the influence of prey depth and implications for temporal access to prey,” J. Mammal., vol. 99, no. 1, pp. 27–40, Feb. 2018, doi: 10.1093/jmammal/gyx170.

[16]     R. H. MacArthur and E. R. Pianka, “On Optimal Use of a Patchy Environment,” Am. Nat., vol. 100, no. 916, pp. 603–609, 1966, doi: 10.1086/282454.

[17]     C. Fontaine, C. L. Collin, and I. Dajoz, “Generalist foraging of pollinators: diet expansion at high density,” J. Ecol., vol. 96, no. 5, pp. 1002–1010, 2008, doi: 10.1111/j.1365-2745.2008.01405.x.

[18]     R. Costa-Pereira, V. H. W. Rudolf, F. L. Souza, and M. S. Araújo, “Drivers of individual niche variation in coexisting species,” J. Anim. Ecol., vol. 87, no. 5, pp. 1452–1464, 2018, doi: 10.1111/1365-2656.12879.

[19]     M. M. Pires, P. R. Guimarães Jr, M. S. Araújo, A. A. Giaretta, J. C. L. Costa, and S. F. dos Reis, “The nested assembly of individual-resource networks,” J. Anim. Ecol., vol. 80, no. 4, pp. 896–903, 2011, doi: 10.1111/j.1365-2656.2011.01818.x.

[20]     M. S. Araújo, D. I. Bolnick, and C. A. Layman, “The ecological causes of individual specialisation,”Ecol. Lett., vol. 14, no. 9, pp. 948–958, 2011, doi: https://doi.org/10.1111/j.1461-0248.2011.01662.x.

[21]     C. E. Sheppard, R. Heaphy, M. A. Cant, and H. H. Marshall, “Individual foraging specialization in group-living species,” Anim. Behav., vol. 182, pp. 285–294, Dec. 2021, doi: 10.1016/j.anbehav.2021.10.011.

[22]     S. Wild, S. J. Allen, M. Krützen, S. L. King, L. Gerber, and W. J. E. Hoppitt, “Multi-network-based diffusion analysis reveals vertical cultural transmission of sponge tool use within dolphin matrilines,” Biol. Lett., vol. 15, no. 7, p. 20190227, Jul. 2019, doi: 10.1098/rsbl.2019.0227.

[23]     L. M. Aplin, D. R. Farine, J. Morand-Ferron, A. Cockburn, A. Thornton, and B. C. Sheldon, “Experimentally induced innovations lead to persistent culture via conformity in wild birds,” Nature, vol. 518, no. 7540, pp. 538–541, Feb. 2015, doi: 10.1038/nature13998.

[24]     E. Van de Waal, C. Borgeaud, and A. Whiten, “Potent Social Learning and Conformity Shape a Wild Primate’s Foraging Decisions,” Science, Apr. 2013, doi: 10.1126/science.1232769.

[25]     D. I. Bolnick et al., “Why intraspecific trait variation matters in community ecology,” Trends Ecol. Evol., vol. 26, no. 4, pp. 183–192, Apr. 2011, doi: 10.1016/j.tree.2011.01.009.

The costs and benefits of automated behavior classification

Clara Bird, PhD Student, OSU Department of Fisheries, Wildlife, and Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

“Why don’t you just automate it?” This is a question I am frequently asked when I tell someone about my work. My thesis involves watching many hours of drone footage of gray whales and meticulously coding behaviors, and there are plenty of days when I have asked myself that very same question. Streamlining my process is certainly appealing and given how wide-spread and effective machine learning methods have become, it is a tempting option to pursue. That said, machine learning is only appropriate for certain research questions and scales, and it’s important to consider these before investing in using a new tool.

The application of machine learning methods to behavioral ecology is called computational ethology (Anderson & Perona, 2014). To identify behaviors from videos, the model tracks individuals across video frames and identifies patterns of movement that form a behavior. This concept is similar to the way we identify a whale as traveling if it’s moving in a straight line and as foraging if it’s swimming in circles within a small area (Mayo & Marx, 1990, check out this blog to learn more). The level of behavioral detail that the model is able to track  depends on the chosen method (Figure 1, Pereira et al., 2020). These methods range from tracking each animal as a simple single point (called a centroid) to tracking the animal’s body positioning in 3D (this method is called pose estimation), which range from providing less detailed to more detailed behavior definitions. For example, tracking an individual as a centroid could be used to classify traveling and foraging behaviors, while pose estimation could identify specific foraging tactics. 

Figure 1. Figure from Pereira et al. (2020) illustrating the different methods of animal behavior tracking that are possible using machine learning.

Pose estimation involves training the machine learning algorithm to track individual anatomical features of an individual (e.g., the head, legs, and tail of a rat), meaning that it can define behaviors in great detail. A behavior state could be defined as a combination of the angle between the tail and the head, and the stride length. 

For example, Mearns et al. (2020) used pose estimation to study how zebrafish larvae in a lab captured their prey. They tracked the tail movements of individual larvae when presented with prey and classified these movements into separate behaviors that allowed them to associate specific behaviors with prey capture (Figure 2). The authors found that these behaviors occurred in a specific sequence, that the behaviors kept the prey within the larvae’s line of sight, and that the sequence was triggered by visual cues.  In fact, when they removed the visual cue of the prey, the larvae terminated the behavior sequence, meaning that the larvae are continually choosing to do each behavior in the sequence, rather than the sequence being one long behavior event that is triggered only by the initial visual cue. This study is a good example of the applicability of machine learning models for questions aimed at kinematics and fine-scale movements. Pose estimation has also been used to study the role of facial expression and body language in rat social communication (Ebbesen & Froemke, 2021). 

Figure 2. Excerpt from figure 1 of Mearns et al. (2020) illustrating (A) the camera set up for their experiment, (B) how the model tracked the eye angles and tail of the larvae fish, (C) the kinematics extracted from the footage. In panel (C) the top plot shows how the eyes converged on the same object (the prey) during prey capture event, the middle plot shows when the tail was curved to the left or the right, and the bottom plot shows the angle of the tail tip relative to the body.

While previous machine learning methods to track animal movements required individuals to be physically marked, the current methods can perform markerless tracking (Pereira et al., 2020). This improvement has broadened the kinds of studies that are possible. For example, Bozek et al., (2021) developed a model that tracked individuals throughout an entire honeybee colony and showed that certain individual behaviors were spatially distributed within the colony (Figure 3). Machine learning enabled the researchers to track over 1000 individual bees over several months, a task that would be infeasible for someone to do by hand. 

Figure 3. Excerpt from figure 1 of Bozek et al., (2021) showing how individual bees and their trajectories were tracked.

These studies highlight that the potential benefits of using machine learning when studying fine scale behaviors (like kinematics) or when tracking large groups of individuals. Furthermore, once it’s trained, the model can process large quantities of data in a standardized way to free up time for the scientists to focus on other tasks.

While machine learning is an exciting and enticing tool, automating behavior detection via machine learning could be its own PhD dissertation. Like most things in life, there are costs and benefits to using this technique. It is a technically difficult tool, and while applications exist to make it more accessible, knowledge of the computer science behind it is necessary to apply it effectively and correctly. Secondly, it can be tedious and time consuming to create a training dataset for the model to “learn” what each behavior looks like, as this step involves manually labeling examples for the model to use. 

As I’ve mentioned in a previous blog, I came quite close to trying to study the kinematics of gray whale foraging behaviors but ultimately decided that counting fluke beats wasn’t necessary to answer my behavioral research questions. It was important to consider the scale of my questions (as described in Allison’s blog) and I think that diving into more fine-scale kinematics questions could be a fascinating follow-up to the questions I’m asking in my PhD. 

For instance, it would be interesting to quantify how gray whales use their flukes for different behavior tactics. Do gray whales in better body condition beat their flukes more frequently while headstanding? Does the size of the fluke affect how efficiently they can perform certain tactics? While these analyses would help quantify the energetic costs of different behaviors in better detail, they aren’t necessary for my broad scale questions. Consequently, taking the time to develop and train a pose estimation machine learning model is not the best use of my time.

That being said, I am interested in applying machine learning methods to a specific subset of my dataset. In social behavior, it is not only useful to quantify the behaviors exhibited by each individual but also the distance between them. For example, the distance between a mom and her calf can be indicative of the calves’ dependence on its mom (Nielsen et al., 2019). However, continuously measuring the distance between two individuals throughout a video is tedious and time intensive, so training a machine learning model could be an effective use of time. I plan to work with an intern this summer to develop a machine learning model to track the distance between pairs of gray whales in our drone footage and then relate this distance data with the manually coded behaviors to examine patterns in social behavior (Figure 4).  Stay tuned to learn more about our progress!

Figure 4. A mom and calf pair surfacing together. Image collected under NOAA/NMFS permit #21678

Did you enjoy this blog? Want to learn more about marine life, research, and conservation? Subscribe to our blog and get a weekly alert when we make a new post! Just add your name into the subscribe box on the left panel.  

References

Anderson, D. J., & Perona, P. (2014). Toward a Science of Computational Ethology. Neuron, 84(1), 18–31. https://doi.org/10.1016/j.neuron.2014.09.005

Bozek, K., Hebert, L., Portugal, Y., Mikheyev, A. S., & Stephens, G. J. (2021). Markerless tracking of an entire honey bee colony. Nature Communications, 12(1), 1733. https://doi.org/10.1038/s41467-021-21769-1

Ebbesen, C. L., & Froemke, R. C. (2021). Body language signals for rodent social communication. Current Opinion in Neurobiology, 68, 91–106. https://doi.org/10.1016/j.conb.2021.01.008

Mayo, C. A., & Marx, M. K. (1990). Surface foraging behaviour of the North Atlantic right whale, Eubalaena glacialis , and associated zooplankton characteristics. Canadian Journal of Zoology, 68(10), 2214–2220. https://doi.org/10.1139/z90-308

Mearns, D. S., Donovan, J. C., Fernandes, A. M., Semmelhack, J. L., & Baier, H. (2020). Deconstructing Hunting Behavior Reveals a Tightly Coupled Stimulus-Response Loop. Current Biology, 30(1), 54-69.e9. https://doi.org/10.1016/j.cub.2019.11.022

Nielsen, M., Sprogis, K., Bejder, L., Madsen, P., & Christiansen, F. (2019). Behavioural development in southern right whale calves. Marine Ecology Progress Series, 629, 219–234. https://doi.org/10.3354/meps13125

Pereira, T. D., Shaevitz, J. W., & Murthy, M. (2020). Quantifying behavior to understand the brain. Nature Neuroscience, 23(12), 1537–1549. https://doi.org/10.1038/s41593-020-00734-z

Of snakes and whales: How food availability and body condition affect reproduction

Clara Bird, PhD Student, OSU Department of Fisheries, Wildlife, and Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

Over six field seasons the GEMM lab team has conducted nearly 500 drone flights over gray whales, equaling over 100 hours of footage. These hours of footage are the central dataset for my PhD dissertation, so it’s up to me to process them all. This process can be challenging, tedious, and daunting, but it is also quite fun and a privilege to be the one person who gets to watch all the footage. It’s fascinating to get to know the whales and their behaviors and pick up on patterns. It motivates me to get through this video processing step and start doing the data analysis. Recently, it’s been especially fun to notice patterns that I’ve seen mentioned in the literature. One example is adult social behavior. 

There are two categories of social behavior that I’m interested in studying: maternal behavior, defined as interactions between a mom and its calf, and general social behaviors, defined as social interactions between non-mom/calf pairs. In this blog I’ll focus on general social behaviors, but if you’re interested in maternal behavior check out this blog. General social behavior, which I’ll refer to as social behavior moving forward, includes tactile interactions and promiscuous behaviors (Torres et al. 2018; Clip 1). While gray whales in the PCFG range are primarily foraging, researchers have observed increases in social behavior towards the end of the foraging season (Stelle et al., 2008; Torres et al., 2018). We think that this indicates that the whales are starting to focus less on feeding and more on breeding. This tradeoff of foraging vs. socializing time is interesting because it comes at an energetic cost.

Clip 1. Example of social interaction between a male and female gray whale off the coast of Oregon, USA. Collected under NOAA/NMFS permit #21678

Broadly, animals need to balance the energetic demands of survival with those of reproduction. They need to reproduce to pass on their genes, but reproduction is energetically demanding, and animals also need to survive and grow to be able to reproduce. The decision to reproduce is costly because reproduction requires energetic investment and time investment since animals do not forage (gaining energy) when they are socializing. Consequently, only animals with sufficient energy reserves (i.e., body condition) to invest in reproduction actually engage in reproduction. Given these costs associated with reproduction, we expect to see a relationship between social behavior and body condition (Green, 2001) with mainly animals in good body condition engaging in social behavior because these animals have sufficient reserves to sustain the cost. Furthermore, since body condition is an indicator of foraging success and prey availability, environmental conditions can also affect social behavior and reproduction through this pathway. 

Rahman et al. (2014) used a lab experiment to study the relationship between nutritional stress and male guppy courtship behavior (Figure 1). In their experiment they tested for the effects of both decreased diet quantity and quality on the frequency of male courtship behaviors. Rahman et al (2014) found that individuals in the low-quantity group were significantly smaller than those in the high-quality group and that diet quantity had a significant effect on the frequency of courtship behaviors. Males fed a low-quantity diet performed fewer courtship behaviors. Interestingly, there was no significant effect of diet quality on courtships behavior, although there was some evidence of an interaction effect, which suggests that within the low-quantity group, males fed with high-quality food performed more courtship behaviors that those fed with low-quality food. This study is interesting because it shows how foraging success (diet quantity and quality) can affect courting behavior. 

Figure 1. A guppy (Rahman et al., 2013)

However, guppies are not the ideal species for comparison to gray whales because gray whales and guppies have quite different life history traits. A more fitting comparison would be with an example species with more in common with gray whales, such as viviparous capital breeders. Viviparous animals develop the embryo inside the body and give live birth. Capital breeders forage to build energy reserves and then rely on those energy reserves during reproduction. Surprisingly, I found asp vipers to be a good example species for comparison to gray whales.

Asp vipers (Figure 2) are viviparous snakes who are considered capital breeders because they forage prior to hibernation, and then begin reproduction immediately following hibernation without additional foraging. Naulleau & Bonnet (1996) conducted a field study on female asp vipers to determine if there was a difference in body condition at the start of the breeding season between females who reproduced or not during that season. To do this they marked individuals and measured their body condition at the start of the breeding season and then recaptured those individuals at the end of the breeding season and recorded whether the individual had reproduced. Interestingly, they found that there was a strongly significant difference in body condition between females that did and did not reproduce. In fact, they discovered that no female below a certain body condition value reproduced, meaning that they found a body condition threshold for reproduction. 

Figure 2. An asp viper

Additionally, a study on water pythons found that their body condition threshold for reproduction shifted over time in response to prey availability (Madsen & Shine, 1999). These authors found that females lowered their threshold after several consecutive years of poor prey availability. These studies are really exciting to me because they address questions that the GRANITE project team is interested in tackling.

Understanding the relationship between body condition and reproduction in gray whales is an important puzzle piece for our work. The aim of the GRANITE project is to understand how the effects of stressors on individual whales scales up to population level impacts (read Lisa’s blog to learn more). Reproduction rates play a big role in population dynamics, so it is important to understand what factors affect reproduction. Since we’re studying these whales on their foraging grounds, assessing body condition provides an important link between foraging behavior and reproduction. 

For example, if an individual’s response to a stressor is to forage less, that may lead to poorer body condition, meaning that they may be less likely to reproduce. While reduced reproduction in one individual may not have a big effect on the population, the same response from multiple individuals could impact the population’s dynamics (i.e., increasing or decreasing abundance). Understanding these different relationships between behavior, body condition, and reproduction rates is a big undertaking, but it’s exciting to be a member of the GRANITE team as this strong group of scientists works to bring together different data streams to work on this big picture question. We’re all deep into data processing right now so stay tuned over the next few years to learn more about gray whale social behavior and to find out if fat whales are more social than skinny whales. 

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References

Green, A. J. (2001). Mass/Length Residuals: Measures of Body Condition or Generators of Spurious Results? Ecology, 82(5), 1473–1483. https://doi.org/10.1890/0012-9658(2001)082[1473:MLRMOB]2.0.CO;2

Madsen, T., & Shine, R. (1999). The adjustment of reproductive threshold to prey abundance in a capital breeder. Journal of Animal Ecology, 68(3), 571–580. https://doi.org/10.1046/j.1365-2656.1999.00306.x

Naulleau, G., & Bonnet, X. (1996). Body Condition Threshold for Breeding in a Viviparous Snake. Oecologia, 107(3), 301–306.

Rahman, M. M., Kelley, J. L., & Evans, J. P. (2013). Condition-dependent expression of pre- and postcopulatory sexual traits in guppies. Ecology and Evolution, 3(7), 2197–2213. https://doi.org/10.1002/ece3.632

Rahman, M. M., Turchini, G. M., Gasparini, C., Norambuena, F., & Evans, J. P. (2014). The Expression of Pre- and Postcopulatory Sexually Selected Traits Reflects Levels of Dietary Stress in Guppies. PLOS ONE, 9(8), e105856. https://doi.org/10.1371/journal.pone.0105856

Stelle, L. L., Megill, W. M., & Kinzel, M. R. (2008). Activity budget and diving behavior of gray whales (Eschrichtius robustus) in feeding grounds off coastal British Columbia. Marine Mammal Science, 24(3), 462–478. https://doi.org/10.1111/j.1748-7692.2008.00205.x

Torres, L. G., Nieukirk, S. L., Lemos, L., & Chandler, T. E. (2018). Drone up! Quantifying whale behavior from a new perspective improves observational capacity. Frontiers in Marine Science, 5(SEP). https://doi.org/10.3389/fmars.2018.00319

Learning the right stuff – examining social transmission in humans, monkeys, and cetaceans

Clara Bird, PhD Student, OSU Department of Fisheries, Wildlife, and Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

The start of a new school year is always an exciting time. Like high school, it means seeing friends again and the anticipation of preparing to learn something new. Even now, as a grad student less focused on coursework, the start of the academic year involves setting project timelines and goals, most of which include learning. As I’ve been reflecting on these goals, one of my dad’s favorite sayings has been at the forefront of my mind. As an overachieving and perfectionist kid, I often got caught up in the pursuit of perfect grades, so the phrase “just learn the stuff” was my dad’s reminder to focus on what matters. Getting good grades didn’t matter if I wasn’t learning. While my younger self found the phrase rather frustrating, I have come to appreciate and find comfort in it. 

Given that my research is focused on behavioral ecology, I’ve also spent a lot of time thinking about how gray whales learn. Learning is important, but also costly. It involves an investment of energy (a physiological cost, Christie & Schrater, 2015; Jaumann et al., 2013), and an investment of time (an opportunity cost). Understanding the costs and benefits of learning can help inform conservation efforts because how an individual learns today affects the knowledge and tactics that the individual will use in the future. 

Like humans, individual animals can learn a variety of tactics in a variety of ways. In behavioral ecology we classify the different types of learning based on the teacher’s role (even though they may not be consciously teaching). For example, vertical transmission is a calf learning from its mom, and horizontal transmission is an individual learning from other conspecifics (individuals of the same species) (Sargeant & Mann, 2009). An individual must be careful when choosing who to learn from because not all strategies will be equally efficient. So, it stands to reason than an individual should choose to learn from a successful individual. Signals of success can include factors such as size and age. An individual’s parent is an example of success because they were able to reproduce (Barrett et al., 2017). Learning in a population can be studied by assessing which individuals are learning, who they are learning from, and which learned behaviors become the most common.

An example of such a study is Barrett et al. (2017) where researchers conducted an experiment on capuchin monkeys in Costa Rica. This study centered around the Panama ́fruit, which is extremely difficult to open and there are several documented capuchin foraging tactics for processing and consuming the fruit (Figure 1). For this study, the researchers worked with a group of monkeys who lived in a habitat where the fruit was not found, but the group included several older members who had learned Panamá fruit foraging tactics prior to joining this group. During a 75-day experiment, the researchers placed fruits near the group (while they weren’t looking) and then recorded the tactics used to process the fruit and who used each tactic. Their results showed that the most efficient tactic became the most common tactic over time, and that age-bias was a contributing factor, meaning that individuals were more like to copy older members of the group. 

Figure 1. Figure from Barrett et al. (2017) showing a capuchin monkey eating a Panamá fruit using the canine seam technique.

Social learning has also been documented in dolphin societies. A long-term study on wild bottlenose dolphins in Shark Bay, Australia assessed how habitat characteristics and the foraging behaviors used by moms and other conspecifics affected the foraging tactics used by calves (Sargeant & Mann, 2009). Interestingly, although various factors predicted what foraging tactic was used, the dominant factor was vertical transmission where the calf used the tactic learned from its mom (Figure 2). Overall, this study highlights the importance of considering a variety of factors because behavioral diversity and learning are context dependent.

Figure 2. Figure from Sargeant & Mann (2009) showing that the probability of a calf using a tactic was higher if the mother used that tactic.

Social learning is something that I am extremely interested in studying in our study population of gray whales in Oregon. While studies on social learning for such long-lived animals require a longer study period than of the span of our current dataset, I still find it important to consider the role learning may play. One day I would love to delve into the different factors of learning by these gray whales and answer questions such as those addressed in the studies I described above. Which foraging tactics are learned? How much of a factor is vertical transmission? Considering that gray whale calves spend the first few months of the foraging season with their mothers I would expect that there is at least some degree of vertical transmission present. Furthermore, how do environmental conditions affect learning? What tactics are learned in good vs. poor years of prey availability? Does it matter which tactic is learned first? While the chances that I’ll get to address these questions in the next few years are low, I do think that investigating how tactic diversity changes across age groups could be a good place to start. As I’ve discussed in a previous blog, my first dissertation chapter will focus on quantifying the degree of individual specialization present in my study group. After reading about age-biased learning, I am curious to see if older whales, as a group, use fewer tactics and if those tactics are the most energetically efficient.

The importance of understanding learning is related to that of studying individual specialization, which can allows us to estimate how behavioral tactics might change in popularity over time and space. We could then combine this with knowledge of how tactics are related to morphology and habitat and the associated energetic costs of each tactic. This knowledge would allow us to estimate the impacts of environmental change on individuals and the population. While my dissertation research only aims to provide a few puzzle pieces in this very large and complicated gray whale ecology puzzle, I am excited to see what I find. Writing this blog has both inspired new questions and served as a good reminder to be more patient with myself because I am still, “just learning the stuff”.

Taking a breather

Allison Dawn, new GEMM Lab Master’s student, OSU Department of Fisheries, Wildlife and Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

While standing at the Stone Shelter at the Saint Perpetua Overlook in 2016, I took in the beauty of one of the many scenic gems along the Pacific Coast Highway. Despite being an East Coast native, I felt an unmistakable draw to Oregon. Everything I saw during that morning’s hike, from the misty fog that enshrouded evergreens and the ocean with mystery, to the giant banana slugs, felt at once foreign and a place I could call home. Out of all the places I visited along that Pacific Coast road trip, Oregon left the biggest impression on me.

Figure 1. View from the Stone Shelter at the Cape Perpetua Overlook, Yachats, OR. June 2016.

For my undergraduate thesis, which I recently defended in May 2021, I researched blue whale surface interval behavior. Surface interval events for oxygen replenishment and rest are a vital part of baleen whale feeding ecology, as it provides a recovery period before they perform their next foraging dive (Hazen et al., 2015; Roos et al., 2016). Despite spending so much time studying the importance of resting periods for mammals, that 2016 road trip was my last true extended resting period/vacation until, several years later in 2021, I took another road trip. This time it was across the country to move to the place that had enraptured me.

Now that I am settled in Corvallis, I have reflected on my journey to grad school and my recent road trip; both prepared me for a challenging and exciting new chapter as an incoming MSc student within the Marine Mammal Institute (MMI).

Part 1: Journey to Grad School

When I took that photo at the Cape Perpetua Overlook in 2016, I had just finished the first two semesters of my undergraduate degree at UNC Chapel Hill. As a first-generation, non-traditional student those were intense semesters as I made the transition from a working professional to full-time undergrad.

By the end of my freshman year I was debating exactly what to declare as my major, when one of my marine science TA’s, Colleen, (who is now Dr. Bove!), advised that I “collect experiences, not degrees.” I wrote this advice down in my day planner and have never forgotten it. Of course, obtaining a degree is important, but it is the experiences you have that help lead you in the right direction.

That advice was one of the many reasons I decided to participate in the Morehead City Field Site program, where UNC undergraduates spend a semester at the coast, living on the Duke Marine Lab’s campus in Beaufort, NC. During that semester, students take classes to fulfill a marine science minor while participating in hands-on research, including an honors thesis project. The experience of designing, carrying out, and defending my own project affirmed that graduate school in the marine sciences was right for me. As I move into my first graduate TA position this fall, I hope to pay forward that encouragement to other undergraduates who are making decisions about their own future path.

Figure 2. Final slide from my honors thesis defense. UNC undergraduates, and now fellow alumni, who participated in the Morehead City Field Site program in Fall 2018.

Part 2: Taking a Breather

Like the GEMM Lab’s other new master’s student Miranda, my road trip covered approximately 2,900 miles. I was solo for much of the drive, which meant there was no one to argue when I decided to binge listen to podcasts. My new favorite is How To Save A Planet, hosted by marine biologist Dr. Ayana Elizabeth Johnson and Alex Blumberg. At the end of each episode they provide a call to action & resources for listeners – I highly recommend this show to anyone interested in what you can do right now about climate change.

Along my trip I took a stop in Utah to visit my parents. I had never been to a desert basin before and engaged in many desert-related activities: visiting Zion National Park, hiking in 116-degree heat, and facing my fear of heights via cliff jumping.

Figure 3. Sandstone Rocks at Sand Hollow National Park, Hurricane, Utah. June 2021.

 My parents wanted to help me settle into my new home, as parents do, so we drove the rest of the way to Oregon together. As this would be their first visit to the state, we strategically planned a trip to Crater Lake as our final scenic stop before heading into Corvallis.

Figure 4. Wizard Island in Crater Lake National Park, Klamath County, OR. June 2021.

This time off was filled with adventure, yet was restorative, and reminded me the importance of taking a break. I feel ready and refreshed for an intense summer of field work.

Part 3: Rested and Ready

Despite accumulating skills to do research in the field over the years, I have yet to do marine mammal field work (or even see a whale in person for that matter.) My mammal research experience included analyzing drone imagery, behind a computer, that had already been captured. As you can imagine, I am extremely excited to join the Port Orford team as part of the TOPAZ/JASPER projects this summer, collecting ecological data on gray whales and their prey. I will be learning the ropes from Lisa Hildebrand and soaking up as much information as possible as I will be taking over as lead for this project next year.

It will take some time before my master’s thesis is fully developed, but it will likely focus on assessing the environmental factors that influence gray whale zooplankton prey availability, and the subsequent impacts on whale movements and health. For five years, the Port Orford project has conducted GoPro drops at 12 sampling stations to collect data on zooplankton relative abundance.

Figures 5 & 6. GEMM GoPro drop stick assembly and footage demonstrating mysid data collection. July 2021.

Paired with this GoPro is a Time-Depth Recorder (TDR) that provides temperature and depth data. The 2021 addition to this GoPro system is a new dissolved oxygen (DO) sensor the GEMM Lab has just acquired. This new piece of equipment will add to the set of parameters we can analyze to describe what and how oceanographic factors drive prey variability and gray whale presence in our study site.My first task as a GEMM Lab student is to get to know this DO sensor, figure out how it works, set it up, test it, attach it to the GoPro device, and prepare it for data collection during the upcoming Port Orford project starting in 1 week!

Figure 7. The GEMM lab’s new RBR solo3 getting ready for Port Orford. July 2021.

Dissolved oxygen plays a vital role in the ocean; however, climate change and increased nutrient loading has caused the ocean to undergo deoxygenation. According to the IUCN’s 2019 Issues Brief, these factors have resulted in an oxygen decline of 2% since the middle of the 20th century, with most of this loss occurring within the first 1000 meters of the ocean. Two percent may not seem like much, but many species have a narrow oxygen threshold and, like pH changes in coral reef systems, even slight changes in DO can have an impact. Additionally, the first 1000 meters of the ocean contains the greatest amount of species richness and biodiversity.

Previous research done in a variety of systems (i.e., estuarine, marine, and freshwater lakes) shows that dissolved oxygen concentrations can have an impact on predator-prey interactions, where low dissolved oxygen results in decreased predation (Abrahams et al., 2007; Breitburg et al., 1997; Domenici et al., 2007; Kramer et al., 1987); and changes in DO also change prey vertical distributions (Decker et al., 2004). In Port Orford, we are interested in understanding the interplay of factors driving zooplankton community distribution and abundance while investigating the trophic interaction between gray whales and their prey.

I have spent some time with our new DO sensor and am looking forward to its first deployments in Port Orford! Stay tuned for updates from the field!

References

Abrahams, M. V., Mangel, M., & Hedges, K. (2007). Predator–prey interactions and changing environments: who benefits?. Philosophical Transactions of the Royal Society B: Biological Sciences, 362(1487), 2095-2104.

Breitburg, D. L., Loher, T., Pacey, C. A., & Gerstein, A. (1997). Varying effects of low dissolved oxygen on trophic interactions in an estuarine food web. Ecological Monographs, 67(4), 489-507.

​​Decker, M. B., Breitburg, D. L., & Purcell, J. E. (2004). Effects of low dissolved oxygen on zooplankton predation by the ctenophore Mnemiopsis leidyi. Marine Ecology Progress Series, 280, 163-172.

Domenici, P., Claireaux, G., & McKenzie, D. J. (2007). Environmental constraints upon locomotion and predator–prey interactions in aquatic organisms: an introduction.

Hazen, E. L., Friedlaender, A. S., & Goldbogen, J. A. (2015). Blue whales (Balaenoptera musculus) optimize foraging efficiency by balancing oxygen use and energy gain as a function of prey density. Science Advances, 1(9), e1500469.

Kramer, D. L. (1987). Dissolved oxygen and fish behavior. Environmental biology of fishes, 18(2), 81-92.

Roos, M. M., Wu, G. M., & Miller, P. J. (2016). The significance of respiration timing in the energetics estimates of free-ranging killer whales (Orcinus orca). Journal of Experimental Biology, 219(13), 2066-2077.