Decisions, decisions: New GEMM Lab publication reveals trade-offs in prey quantity and quality in gray whale foraging

By Lisa Hildebrand, PhD student, OSU Department of Fisheries, Wildlife, & Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

Obtaining enough food is crucial for predators to ensure adequate energy gain for maintenance of vital functions and support for energetically costly life history events (e.g., reproduction). Foraging involves decisions at every step of the process, including prey selection, capture, and consumption, all of which should be as efficient as possible. Making poor foraging decisions can have long-term repercussions on reproductive success and population dynamics (Harris et al. 2007, 2008, Grémillet et al. 2008), and for marine predators that rely on prey that is spatially and temporally dynamic and notoriously patchy (Hyrenbach et al. 2000), these decisions can be especially challenging. Prey abundance and density are frequently used as predictors of marine predator distribution, movement, and foraging effort, with predators often selecting highly abundant or dense prey patches (e.g., Goldbogen et al. 2011, Torres et al. 2020). However, there is increased recognition that prey quality is also an important factor to consider when assessing a predator’s ecology and habitat use (Spitz et al. 2012), and marine predators do show a preference for higher quality prey items (e.g., Haug et al. 2002, Cade et al. 2022). Moreover, negative impacts of low-quality prey on the health and breeding success of some marine mammals (Rosen & Trites 2000, Trites & Donnelly 2003) have been documented. Therefore, examining multiple prey metrics, such as prey quantity and quality, in predator ecology studies is critical.

Figure 1. Site map of the Port Orford TOPAZ/JASPER integrated projects. Blue squares represent the location of the 12 sampling stations within the 2 study sites (site boundaries demarcated with black lines). Brown dot represents the cliff-top observation site where theodolite tracking occurred.

Our integrated TOPAZ/JASPER projects in Port Orford do just this! We collect both prey quantity and quality data from a tandem research kayak, while we track Pacific Coast Feeding Group (PCFG) gray whales from shore. The prey and whale sampling overlap spatially (and often temporally within the same day). This kind of concurrent predator-prey sampling at similar scales is often logistically challenging to achieve, yet because PCFG gray whales have an affinity for nearshore, coastal habitats, it is something we have been able to achieve in Port Orford. Since 2016, a field team comprised of graduate, undergraduate, and high school students has collected data during the month of August to investigate gray whale foraging decisions relative to prey. Every day, a kayak team collects GoPro videos (to assess relative prey abundance; AKA: quantity) and zooplankton samples using a tow net (to assess prey community composition; AKA: quality through caloric content of different species) (Figure 1). At the same time, a cliff team surveys for gray whales from shore and tracks them using a theodolite, which provides us with tracklines of individual whales; We categorize each location of a whale into three broad behavior states (feeding, searching, transiting) based on movement patterns. Over the years, the various students who have participated in the TOPAZ/JASPER projects have written many blog posts, which I encourage you to read here (particularly to get more detailed information about the field methods). 

Figure 2. An example daily layer of relative prey abundance (increasing color darkness corresponds with increasing abundance) in one study site with a whale theodolite trackline recorded on the same day overlaid and color-coded by behavioral state.

Several years of data are needed to conduct a robust analysis for our ecological questions about prey choice, but after seven years, we finally had the data and I am excited to share the results, which are due to the many years of hard work from many students! Our recent paper in Marine Ecology Progress Series aimed to determine whether PCFG gray whale foraging decisions are driven by prey quantity (abundance) or quality (caloric content of species) at a scale of 20 m (which is slightly less than 2 adult gray whale body lengths). In this study, we built upon results from my previous Master’s publication, which revealed that there are significant differences in the caloric content between the six common nearshore zooplankton prey species that PCFG gray whales feed on (Hildebrand et al. 2021). Therefore, in this study we addressed the hypothesis that individual whales will select areas where the prey community is dominated by the mysid shrimp Neomysis rayii, since it is significantly higher in caloric content than the other two prey species we identified, Holmesimysis sculpta (a medium quality mysid shrimp species) and Atylus tridens (a low quality amphipod species) (Hildebrand et al. 2021). We used spatial statistics and model to make daily maps of prey abundance and quality that we compared to our whale tracks and behavior from the same day. Please read our paper for the details on our novel methods that produced a dizzying amount of prey layers, which allowed us to tease apart whether gray whales target prey quantity, quality, or a mixture of both when they forage. 

Figure 3. Figure shows the probability of gray whale foraging relative to prey abundance (color-coded by prey species). Dark grey vertical line represents the mean threshold for the H. sculpta curves (12.0); light grey vertical lines: minimum (7.2) and maximum (15.3) thresholds for the H. sculpta curves. Inflection points could not be calculated for the N. rayii curves

So, what did we find? The models proved our hypothesis wrong: foraging probability was significantly correlated with the quantity and quality of the mysid H. sculpta, which has significantly lower calories than N. rayii. This result puzzled us, until we started looking at the overall quantity of these two prey types in the study area and realized that the amount of calorically-rich N. rayii never reached a threshold where it was beneficial for gray whales to forage. But, there was a lot of H. sculpta, which likely made for an energetic gain for the whales despite not being as calorically rich as N. rayii. We determined a threshold of H. sculpta relative abundance that is required to initiate the gray whale foraging behavior, and the abundance of N. rayii never came close to this level (Figure 3). Despite not having the highest quality, H. sculpta did have the highest abundance and showed a significant positive relationship with foraging behavior, unlike the other prey items. Interestingly, whales never selected areas dominated by the low-calorie species A. tridens. These results demonstrate trade-off choices by whales for this abundant, medium-quality prey.

To our knowledge, individual baleen whale foraging decisions relative to available prey quantity and quality have not been addressed previously at this very fine-scale. Interestingly, this trade-off between prey quantity and quality has also been detected in humpback whales foraging in Antarctica at depths deeper than where the densest krill patches occur; while the whales are exploiting less dense krill patches, these krill composed of larger, gravid, higher-quality krill (Cade et al. 2022). While it is unclear how baleen whales differentiate between prey species or reproductive stages, several mechanisms have been suggested, including visual and auditory identification (Torres 2017). We assume here that gray whales, and other baleen whale species, can differentiate between prey species. Thus, our results showcase the importance of knowing the quality (such as caloric content) of prey items available to predators to understand their foraging ecology (Spitz et al. 2012). 

References

Cade DE, Kahane-Rapport SR, Wallis B, Goldbogen JA, Friedlaender AS (2022) Evidence for size-selective pre- dation by Antarctic humpback whales. Front Mar Sci 9:747788

Goldbogen JA, Calambokidis J, Oleson E, Potvin J, Pyenson ND, Schorr G, Shadwick RE (2011) Mechanics, hydrody- namics and energetics of blue whale lunge feeding: effi- ciency dependence on krill density. J Exp Biol 214:131−146

Grémillet D, Pichegru L, Kuntz G, Woakes AG, Wilkinson S, Crawford RJM, Ryan PG (2008) A junk-food hypothesis for gannets feeding on fishery waste. Proc R Soc B 275: 1149−1156

Harris MP, Beare D, Toresen R, Nøttestad L, and others (2007) A major increase in snake pipefish (Entelurus aequoreus) in northern European seas since 2003: poten- tial implications for seabird breeding success. Mar Biol 151:973−983

Harris MP, Newell M, Daunt F, Speakman JR, Wanless S (2008) Snake pipefish Entelurus aequoreus are poor food for seabirds. Ibis 150:413−415

Haug T, Lindstrøm U, Nilssen KT (2002) Variations in minke whale (Balaenoptera acutorostrata) diet and body condi- tion in response to ecosystem changes in the Barents Sea. Sarsia 87:409−422

Hildebrand L, Bernard KS, Torres LG (2021) Do gray whales count calories? Comparing energetic values of gray whale prey across two different feeding grounds in the eastern North Pacific. Front Mar Sci 8:1008

Hyrenbach KD, Forney KA, Dayton PK (2000) Marine pro- tected areas and ocean basin management. Aquat Con- serv 10:437−458

Rosen DAS, Trites AW (2000) Pollock and the decline of Steller sea lions: testing the junk-food hypothesis. Can J Zool 78:1243−1250

Spitz J, Trites AW, Becquet V, Brind’Amour A, Cherel Y, Galois R, Ridoux V (2012) Cost of living dictates what whales, dolphins and porpoises eat: the importance of prey quality on predator foraging strategies. PLOS ONE 7:e50096

Torres LG, Barlow DR, Chandler TE, Burnett JD (2020) Insight into the kinematics of blue whale surface forag- ing through drone observations and prey data. PeerJ 8: e8906

Torres LG (2017) A sense of scale: foraging cetaceans’ use of scale-dependent multimodal sensory systems. Mar Mamm Sci 33:1170−1193

Trites AW, Donnelly CP (2003) The decline of Steller sea lions Eumetopias jubatus in Alaska: a review of the nutri- tional stress hypothesis. Mammal Rev 33:3−28

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 Biotelemetry1(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 Biology26(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 Evolution2(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 Ecology31(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 Physiology158(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. Physiology34, 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 Science5, 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 Ecology89(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 Series629, 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

A Hundred and One Data Visualizations: What We Can Infer about Gray Whale Health Using Public Data

By Braden Adam Vigil, Oregon State University Undergraduate, GEMM Lab NSF REU Intern

Introduction

My name is Braden Vigil, and I am enjoying this summer with the company of Lisa Hildebrand and Dr. Leigh Torres as a National Science Foundation (NSF) Research Experience for Undergraduates (REU) intern. By slicing off a manageable chunk of the GRANITE project to focus on, I’ve had the chance to explore my passion for data visualization. My excitement for biological research was instilled in me by an impactful high school biology teacher (thank you Mr. Villalobos!) and was narrowed to marine biology research after a chance visit to Oregon State University’s Hatfield Marine Science Center. I’ve come all the way from Southern New Mexico to explore this passion of mine, and the REU program has been one of my first chances to get my feet wet. My advice for any students debating taking big leaps for the sake of passion is to do it – it’s scary, but I’d say there’s nothing better than living out what you want to do (and hopefully getting paid for it!). For this project, the GEMM Lab has saved me the trouble of collecting data – this summer, I’m all action. 

Where Gray Whales Are and Why It Matters

Just as you might find yourself at a grocery store to buy food or at a coffee shop catching up with an old friend, so too do whales have places to go and reasons for being there. Research concerning gray whale ecology – understanding the who, what, when, where, whys – should then have a lot to do with the “where?” and “why?” That’s what my project is about: investigating where the gray whales off the Oregon coast are, and what features of the environment are related to their presence and other aspects of the population. After all, distribution is considered the foundational unit for the biogeographical understanding of a population’s location and its interactions with other species. An example of an environmental driver may be phytoplankton and – subsequently – zooplankton abundance. It’s been shown that bottom-up trophic cascades based on primary productivity directly influence predator and prey populations in both terrestrial and marine ecosystems (Sinclair and Krebs 2002; Benoit-Bird and McManus 2012). This driver specifically could then inform something as significant as population abundance of a predator, though that’s out of the scope of my project. Instead, I’m studying how these environmental drivers, specifically sea water temperature, affects the variation of the thyroid hormone (tri-iodothyronine, T3) in gray whales, which the GEMM Lab quantifies from fecal samples that they non-invasively and opportunistically collect. In terrestrial mammals, T3 is believed to be associated with thermoregulation, yet it is unclear if T3 has the same function in baleen whales who use blubber insulation to thermoregulate. To estimate blubber insulation, we use a proxy, called body area index (BAI) collected via drone footage (Burnett et al. 2018), which you can read more about in Clara’s blog. Insights into variations in T3 hormone levels as related to changes in the environment may allow researchers to better understand thermoregulatory challenges whales face in warming oceans.

This Sounds Like a Lot of Data About the Environment, Where’s it Coming From?

Not only has the GEMM Lab relieved me of the hassle that data collection and fieldwork can be, so too has the Ocean Observatories Initiative (OOI). Starting in 2014, the OOI has set up several buoys off the U.S. West Coast, each equipped with numerous sensors and data-collecting devices. These have been extracting data from the nearby environment since then, including aspects such as dissolved oxygen, pH, and most important to this study, sea temperature. These buoys run deep too! Some devices reach as low as 25 m, which is where we often expect to see whales foraging during surveys. For our interest, there is one specific buoy that is within the GRANITE project’s survey region, the Oregon Inshore Surface Mooring.

Figure 1. Locations of OOI buoys. Blue dots represent buoys, while the yellow dot represents our buoy of interest, the Oregon Inshore Surface Mooring. 

Expectations

The OOI has published, and continues to publish, an unbelievable amount of data. There are many things that would be interesting to investigate, but until we know how much we can bite off versus how much we can chew, we’ve narrowed it down to a few hypotheses we’re currently investigating. 

Table 1. Hypotheses and Expected Results.

A Hundred and One Data Visualizations

As fun as I find testing correlations between variables and creating satisfying looking plots, I must admit that I’m not even halfway into this project and I’ve made a LOT of plots. Plots can be an easy way to understand big datasets and observations. Since not all of the data-collecting devices on the OOI data are continuously running, I first needed to get an idea of how much data we have to work with, and how much of that data overlaps in time with our annual gray whale survey period (June 1 – October 15). Some of these preliminary plots look like Figure 2. In addition, these plots grant us an idea of how variable sea surface temperatures have been in these past few years. Marine heatwaves have occurred recently in the Pacific Ocean and off the U.S. West Coast, and it is important to know if their effects continue to linger to the present. Other, unexplained peaks might also be worth investigating. 

Figure 2. Preliminary plot comparing sea surface temperature data over time, from around June 2016 to December 2021. Straight lines between December to June each year indicates no data, as we have removed these periods from our analysis. 

The goal here is to eventually compare the variables of sea temperature to the T3 hormone levels in gray whales foraging off the Oregon coast. Before this step, it is important to decide what depth of temperature readings are most appropriate to assess. I’ve made several correlation plots of sea  temperature between varying depths of 1 m, 7 m, and 25 m. One such plot is included below (Figure 3). This plot shows variation of temperature between different depths. If there is strong variation between the depths of 1 m and 25 m, then the water column may be well stratified, meaning that gray whale response to environmental temperature may be distinct between these distances, possibly even between 1 m and 7 m. 

Figure 3. Sea surface temperature at 1 m versus 25 m in degrees Celsius, with points color coded by year. 

Conclusion

As previously described, this study plays part into the larger GRANITE project with the goal to understand and make predictions about the ecology and physiology of the gray whale population off of the U.S. West Coast. This study will investigate the significance of sea temperature on aspects of whale health – so far including BAI and T3 hormone level. I will be pursuing a stronger grasp on the variation of these relationships through ongoing analysis. My results should be used to clarify nodes and the correlation between them in the web of dynamics encircling the population. This project has given me great insight into how raw data can be turned into meaningful understandings and subsequent impacts. The public OOI data is a scattershot of many different measurements using many different devices constantly. The answers/solutions to the conservation of species threatened by the Anthropocene are out there, all that’s required is that we harness them. 

References

Benoit-Bird, K. J., & McManus, M. A. (2012). Bottom-up regulation of a pelagic community through spatial aggregations. Biology Letters8(5), 813–816. https://doi.org/10.1098/rsbl.2012.0232

Burnett, J. D., & Wing, M. G. (2018). A low-cost near-infrared digital camera for fire detection and monitoring. International Journal of Remote Sensing39(3), 741–753. https://doi.org/10.1080/01431161.2017.1385109

Sinclair, A. R. E., & Krebs, C. J. (2002). Complex numerical responses to top–down and bottom–up processes in vertebrate populations. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences357(1425), 1221–1231.https://doi.org/10.1098/rstb.2002.1123.

Harbor porpoise and gray whale distribution over three decades: introducing the EMERALD project

By Dawn Barlow, Postdoctoral Scholar, OSU Department of Fisheries, Wildlife, and Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

Throughout the world, humans rely on coastal regions for shipping and commerce, fisheries, industrial development, and increasingly for the development of marine renewable energy such as wind and wave energy [1]. Nearshore environments, including the coastal waters of the Northern California Current (NCC), are therefore coupled social-ecological systems, at the intersection of human and biological productivity [2].

The NCC supports a diverse food web of ecologically and commercially important species [3]. The nearshore region of the NCC is further shaped by a rich mosaic of complex features including rocky reefs, kelp forests, and sloping sandy bottom substrate [4], creating habitat for numerous species of conservation interest, including invertebrates, fish, seabirds, and marine mammals [5]. Despite its importance, this realm poses significant challenges for vessel-based data collection, and therefore it remains relatively poorly monitored and understood.

The view from Cape Foulweather, showing the complex mosaic of nearshore habitat features. Photo: D. Barlow.

I am excited to introduce a new project focused on these important nearshore waters, in which we will be Examining Marine mammal Ecology through Region-wide Assessment of Long-term Data (EMERALD). Since 1992, standardized surveys have been conducted between San Francisco Bay, CA, and the Columbia River, OR, to monitor the abundance of marbled murrelets, a seabird of conservation concern. Each spring and summer, researchers have simultaneously been diligently documenting the locations of harbor porpoise and gray whale sightings—two iconic marine mammal species that rely on the nearshore waters of the NCC. This rich and extensive record is rare for marine mammal data, particularly in the challenging, turbulent nearshore environment. Furthermore, harbor porpoises are cryptic, making visual sampling particularly challenging, and gray whales can be sparsely distributed, yielding low sample sizes in the absence of long-term data collection.

Left: The survey team collecting data; Right: Marbled murrelet floating on the water.

For the EMERALD project, we will investigate spatial and temporal distribution patterns of harbor porpoises and gray whales in relation to fluctuations in key environmental drivers. The primary goals of the project are to (1) Identify persistent hotspots in harbor porpoise and gray whale sightings over time, and (2) Examine the environmental drivers of sighting hotspots through spatial and temporal analyses.

A harbor porpoise surfacing off the central Oregon coast. Photo: L. Torres.

From a first look at the data, we are already excited by some emerging patterns. In total, the dataset contains sightings of 6,763 harbor porpoise (mean 233 per year) and 530 gray whales (mean 18 per year). Preliminary data exploration reveals that harbor porpoise sightings increased in 2011-2012, predominantly between Cape Blanco, OR, and Cape Mendocino, CA. Gray whale sightings appear to follow an oscillating, cyclical pattern with peaks approximately every three years, with notable disruption of this pattern during the marine heatwave of 2014-2015. What are the drivers of sighting hotspots and spatial and temporal fluctuations in sighting rates? Time—and a quantitative analytical approach involving density estimation, timeseries analysis, and species distribution modeling—will tell.

A gray whale forages in kelp forest habitat over a nearshore rocky reef. Photo: T. Chandler.

I recently completed my PhD on the ecology and distribution of blue whales in New Zealand (for more information, see the OBSIDIAN project). Now, I am excited to apply the spatial analysis skills have been honing to a new study system and two new study species as I take on a new role in the GEMM Lab as a Postdoctoral Scholar. The EMERALD project will turn my focus to the nearshore waters close to home that I have grown to love over the past six years as a resident of coastal Oregon. The surveys I will be working with began before I was born, and I am truly fortunate to inherit such a rich dataset—a rare treat for a marine mammal biologist, and an exciting prospect for a statistical ecologist.

Dawn and Quin the dog, enjoying views of Oregon’s complex and important nearshore waters. Both are thrilled to remain in Oregon for the EMERALD project. Photo: R. Kaplan.

So, stay tuned for our findings as the project unfolds. In the meantime, I want express gratitude to Craig Strong of Crescent Coastal Research who has led the dedicated survey effort for the marbled murrelet monitoring program, without whom none of the data would exist. This project is funded by the Oregon Gray Whale License Plate funds, and we thank the gray whale license plate holders for their support of marine mammal research.

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References:

1.        Jouffray, J.-B., Blasiak, R., Norström, A. V., Österblom, H., and Nyström, M. (2020). The Blue Acceleration: The Trajectory of Human Expansion into the Ocean. One Earth 2, 43–54.

2.        Sjostrom, A.J.C., Ciannelli, L., Conway, F., and Wakefield, W.W. (2021). Gathering local ecological knowledge to augment scientific and management understanding of a living coastal resource: The case of Oregon’s nearshore groundfish trawl fishery. Mar. Policy 131, 104617.

3.        Bograd, S.J., Schroeder, I., Sarkar, N., Qiu, X., Sydeman, W.J., and Schwing, F.B. (2009). Phenology of coastal upwelling in the California Current. Geophys. Res. Lett. 36, 1–5.

4.        Romsos, G., Goldfinger, C., Robison, R., Milstein, R., Chaytor, J., and Wakefield, W. (2007). Development of a regional seafloor surficial geologic habitat map for the continental margins of Oregon and Washington, USA. Mapp. Seafloor Habitat Charact. Geol. Assoc. Canada, Spec. Pap., 219–243.

5.        Oregon Department of Fish and Wildlife (2016). Oregon Nearshore Strategy. Available at: https://oregonconservationstrategy.org/oregon-nearshore-strategy/ [Accessed January 10, 2022].

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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Reuniting with some old friends: The 8th GRANITE field season is underway

By Lisa Hildebrand, PhD student, OSU Department of Fisheries & Wildlife, Geospatial Ecology of Marine Megafauna Lab

We are almost halfway through June which means summer has arrived! Although, here on the Oregon coast, it does not entirely feel like it. We have been swinging between hot, sunny days and cloudy, foggy, rainy days that are reminiscent of those in spring or even winter. Despite these weather pendulums, the GEMM Lab’s GRANITE project is off to a great start in its 8th field season! The field team has already ventured out onto the Pacific Ocean in our trusty RHIB Ruby on four separate days looking for gray whales and in this blog post, I am going to share what we have seen so far.

The core GRANITE field team before the May 24th “trial run”. From left to right: Leigh Torres, KC Bierlich, Clara Bird, Lisa Hildebrand, Alejandro Fernández Ajó. Source: L. Torres.

PI Leigh, PhD candidate Clara and I headed out for a “trial run” on May 24th. While the intention for the day was to make sure all our gear was running smoothly and we still remembered how to complete the many tasks associated with our field work (boat loading and trailering, drone flying and catching, poop scooping, data download, to name a few), we could not resist surveying our entire study range given the excellent conditions. It was a day that all marine field scientists hope for – low winds (< 5 kt all day) and a 3 ft swell over a long period. Despite surveying between Waldport and Depoe Bay, we only encountered one whale, but it was a whale that put a smile on each of our faces. After “just” 252 days, we reunited with Solé, the star of our GRANITE dataset, with record numbers of fecal samples and drone flights collected. This record is due to what seems to be a strong habitat or foraging tactic preference by Solé to remain in a relatively small spatial area off the Oregon coast for most of the summer, rather than traveling great swaths of the coast in search for food. Honest truth, on May 24th we found her exactly where we expected to find her. While we did not collect a fecal sample from her on that day, we did perform a drone flight, allowing us to collect a critical early feeding season data point on body condition. We hope that Solé has a summer full of mysids on the Oregon coast and that we will be seeing her often, getting rounder each time!

Our superstar whale Solé. Her identifying features are a small white line on her left side (green box) and a white dot in front of her dorsal hump on the right side (red circle). Source: GEMM Lab. Photograph captured under NOAA/NMFS permit #21678

Just a week after this trial day, we had our official start to the field season with back-to-back days on the water. On our first day, postdoc Alejandro, Clara and I were joined by St. Andrews University Research Fellow Enrico Pirotta, who is another member of the GRANITE team. Enrico’s role in the GRANITE project is to implement our long-term, replicate dataset into a framework called Population consequences of disturbance (PCoD; you can read all about it in a previous blog). We were thrilled that Enrico was able to join us on the water to get a sense for the species and system that he has spent the last several months trying to understand and model quantitatively from a computer halfway across the world. Luckily, the whales sure showed up for Enrico, as we saw a total of seven whales, all of which were known individuals to us! Several of the whales were feeding in water about 20 m deep and surfacing quite erratically, making it hard to get photos of them at times. Our on-board fish finder suggested that there was a mid-water column prey layer that was between 5-7 m thick. Given the flat, sandy substrate the whales were in, we predicted that these layers were composed of porcelain crab larvae. Luckily, we were able to confirm our hypothesis immediately by dropping a zooplankton net to collect a sample of many porcelain crab larvae. Porcelain crab larvae have some of the lowest caloric values of the nearshore zooplankton species that gray whales likely feed on (Hildebrand et al. 2021). Yet, the density of larvae in these thick layers probably made them a very profitable meal, which is likely the reason that we saw another five whales the next day feeding on porcelain crab larvae once again.

On our most recent field work day, we only encountered Solé, suggesting that the porcelain crab swarms had dissipated (or had been excessively munched on by gray whales), and many whales went in search for food elsewhere. We have done a number of zooplankton net tows across our study area and while we did collect a good amount of mysid shrimp already, they were all relatively small. My prediction is that once these mysids grow to a more profitable size in a few days or weeks, we will start seeing more whales again.

The GRANITE team from above, waiting & watching for whales, as we will be doing for the rest of the summer! Source: GEMM Lab.

So far we have seen nine unique individuals, flown the drone over eight of them, collected fecal samples from five individuals, conducted 10 zooplankton net tows and seven GoPro drops in just four days of field work! We are certainly off to a strong start and we are excited to continue collecting rock solid GRANITE data this summer to continue our efforts to understand gray whale ecology and physiology.

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Literature cited

Hildebrand L, Bernard KS, Torres LGT. 2021. Do gray whales count calories? Comparing energetic values of gray whale prey across two different feeding grounds in the Eastern North Pacific. Frontiers in Marine Science 8. doi: 10.3389/fmars.2021.683634

New publication by GEMM Lab reveals sub-population health differences in gray whales 

Dr. KC Bierlich, Postdoctoral Scholar, OSU Department of Fisheries, Wildlife, & Conservation Sciences, Geospatial Ecology of Marine Megafauna (GEMM) Lab

In a previous blog, I discussed the importance of incorporating measurement uncertainty in drone-based photogrammetry, as drones with different sensors, focal length lenses, and altimeters will have varying levels of measurement accuracy. In my last blog, I discussed how to incorporate photogrammetric uncertainty when combining multiple measurements to estimate body condition of baleen whales. In this blog, I will highlight our recent publication in Frontiers in Marine Science (https://doi.org/10.3389/fmars.2022.867258) led by GEMM Lab’s Dr. Leigh TorresClara Bird, and myself that used these methods in a collaborative study using imagery from four different drones to compare gray whale body condition on their breeding and feeding grounds (Torres et al., 2022).

Most Eastern North Pacific (ENP) gray whales migrate to their summer foraging grounds in Alaska and the Arctic, where they target benthic amphipods as prey. A subgroup of gray whales (~230 individuals) called the Pacific Coast Feeding Group (PCFG), instead truncates their migration and forages along the coastal habitats between Northern California and British Columbia, Canada (Fig. 1). Evidence from a recent study lead by GEMM Lab’s Lisa Hildebrand (see this blog) found that the caloric content of prey in the PCFG range is of equal or higher value than the main amphipod prey in the Arctic/sub-Arctic regions (Hildebrand et al., 2021). This implies that greater prey density and/or lower energetic costs of foraging in the Arctic/sub-Arctic may explain the greater number of whales foraging in that region compared to the PCFG range. Both groups of gray whales spend the winter months on their breeding and calving grounds in Baja California, Mexico. 

Figure 1. The GEMM Lab field team following a Pacific Coast Feeding Group (PCFG) gray whale swimming in a kelp bed along the Oregon Coast during the summer foraging season. 

In January 2019 an Unusual Mortality Event (UME) was declared for gray whales due to the elevated numbers of stranded gray whales between Mexico and the Arctic regions of Alaska. Most of the stranded whales were emaciated, indicating that reduced nutrition and starvation may have been the causal factor of death. It is estimated that the population dropped from ~27,000 individuals in 2016 to ~21,000 in 2020 (Stewart & Weller, 2021).

During this UME period, between 2017-2019, the GEMM Lab was using drones to monitor the body condition of PCFG gray whales on their Oregon coastal feeding grounds (Fig. 1), while Christiansen and colleagues (2020) was using drones to monitor gray whales on their breeding grounds in San Ignacio Lagoon (SIL) in Baja California, Mexico. We teamed up with Christiansen and colleagues to compare the body condition of gray whales in these two different areas leading up to the UME. Comparing the body condition between these two populations could help inform which population was most effected by the UME.

The combined datasets consisted of four different drones used, thus different levels of photogrammetric uncertainty to consider. The GEMM Lab collected data using a DJI Phantom 3 Pro, DJI Phantom 4, and DJI Phantom 4 Pro, while Christiansen et al., (2020) used a DJI Inspire 1 Pro. By using the methodological approach described in my previous blog (here, also see Bierlich et al., 2021a for more details), we quantified photogrammetric uncertainty specific to each drone, allowing cross-comparison between these datasets. We also used Body Area Index (BAI), which is a standardized relative measure of body condition developed by the GEMM Lab (Burnett et al., 2018) that has low uncertainty with high precision, making it easier to detect smaller changes between individuals (see blog here, Bierlich et al., 2021b). 

While both PCFG and ENP gray whales visit San Ignacio Lagoon in the winter, we assume that the photogrammetry data collected in the lagoon is mostly of ENP whales based on their considerably higher population abundance. We also assume that gray whales incur low energetic cost during migration, as gray whale oxygen consumption rates and derived metabolic rates are much lower during migration than on foraging grounds (Sumich, 1983). 

Interestingly, we found that gray whale body condition on their wintering grounds in San Ignacio Lagoon deteriorated across the study years leading up to the UME (2017-2019), while the body condition of PCFG whales on their foraging grounds in Oregon concurrently increased. These contrasting trajectories in body condition between ENP and PCFG whales implies that dynamic oceanographic processes may be contributing to temporal variability of prey available in the Arctic/sub-Arctic and PCFG range. In other words, environmental conditions that control prey availability for gray whales are different in the two areas. For the ENP population, this declining nutritive gain may be associated with environmental changes in the Arctic/sub-Arctic region that impacted the predictability and availability of prey. For the PCFG population, the increase in body condition across years may reflect recovery of the NE Pacific Ocean from the marine heatwave event in 2014-2016 (referred to as “The Blob”) that resulted with a period of low prey availability. These findings also indicate that the ENP population was primarily impacted in the die-off from the UME. 

Surprisingly, the body condition of PCFG gray whales in Oregon was regularly and significantly lower than whales in San Ignacio Lagoon (Fig. 2). To further investigate this potential intrinsic difference in body condition between PCFG and ENP whales, we compared opportunistic photographs of gray whales feeding in the Northeastern Chukchi Sea (NCS) in the Arctic collected from airplane surveys. We found that the body condition of PCFG gray whales was significantly lower than whales in the NCS, further supporting our finding that PCFG whales overall have lower body condition than ENP whales that feed in the Arctic (Fig. 3). 

Figure 2. Boxplots showing the distribution of Body Area Index (BAI) values for gray whales imaged by drones in San Ignacio Lagoon (SIL), Mexico and Oregon, USA. The data is grouped by phenology group: End of summer feeding season (departure Oregon vs. arrival SIL) and End of wintering season (arrival Oregon vs. departure SIL). The group median (horizontal line), interquartile range (IQR, box), maximum and minimum 1.5*IQR (vertical lines), and outliers (dots) are depicted in the boxplots. The overlaid points represent the mean of the posterior predictive distribution for BAI of an individual and the bars represents the uncertainty (upper and lower bounds of the 95% HPD interval). Note how PCFG whales at then end of the feeding season (dark green) typically have lower body condition (as BAI) compared to ENP whales at the end of the feeding season when they arrive to SIL after migration (light brown).
Figure 3. Boxplots showing the distribution of Body Area Index (BAI) values of gray whales from opportunistic images collected from a plane in Northeaster Chukchi Sea (NCS) and from drones collected by the GEMM Lab in Oregon. The boxplots display the group median (horizontal line), interquartile range (IQR box), maximum and minimum 1.5*IQR (vertical lines), and outlies (dots). The overlaid points are the BAI values from each image. Note the significantly lower BAI of PCFG whales on Oregon feeding grounds compared to whales feeding in the Arctic region of the NCS.

This difference in body condition between PCFG and ENP gray whales raises some really interesting and prudent questions. Does the lower body condition of PCFG whales make them less resilient to changes in prey availability compared to ENP whales, and thus more vulnerable to climate change? If so, could this influence the reproductive capacity of PCFG whales? Or, are whales that recruit into the PCFG adapted to a smaller morphology, perhaps due to their specialized foraging tactics, which may be genetically inherited and enables them to survive with reduced energy stores?

These questions are on our minds here at the GEMM Lab as we prepare for our seventh consecutive field season using drones to collect data on PCFG gray whale body condition. As discussed in a previous blog by Dr. Alejandro Fernandez Ajo, we are combining our sightings history of individual whales, fecal hormone analyses, and photogrammetry-based body condition to better understand gray whales’ reproductive biology and help determine what the consequences are for these PCFG whales with lower body condition.

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References

Bierlich, K. C., Hewitt, J., Bird, C. N., Schick, R. S., Friedlaender, A., Torres, L. G., … & Johnston, D. W. (2021). Comparing Uncertainty Associated With 1-, 2-, and 3D Aerial Photogrammetry-Based Body Condition Measurements of Baleen Whales. Frontiers in Marine Science, 1729.

Bierlich, K. C., Schick, R. S., Hewitt, J., Dale, J., Goldbogen, J. A., Friedlaender, A.S., et al. (2021b). Bayesian Approach for Predicting Photogrammetric Uncertainty in Morphometric Measurements Derived From Drones. Mar. Ecol. Prog. Ser. 673, 193–210. doi: 10.3354/meps13814

Burnett, J. D., Lemos, L., Barlow, D., Wing, M. G., Chandler, T., & Torres, L. G. (2018). Estimating morphometric attributes of baleen whales with photogrammetry from small UASs: A case study with blue and gray whales. Marine Mammal Science35(1), 108–139.

Christiansen, F., Rodrı́guez-González, F., Martı́nez-Aguilar, S., Urbán, J., Swartz, S., Warick, H., et al. (2021). Poor Body Condition Associated With an Unusual Mortality Event in Gray Whales. Mar. Ecol. Prog. Ser. 658, 237–252. doi:10.3354/meps13585

Hildebrand, L., Bernard, K. S., and Torres, L. G. (2021). Do Gray Whales Count Calories? Comparing Energetic Values of Gray Whale Prey Across Two Different Feeding Grounds in the Eastern North Pacific. Front. Mar. Sci. 8. doi: 10.3389/fmars.2021.683634

Stewart, J. D., and Weller, D. (2021). Abundance of Eastern North Pacific Gray Whales 2019/2020 (San Diego, CA: NOAA/NMFS)

Sumich, J. L. (1983). Swimming Velocities, Breathing Patterns, and Estimated Costs of Locomotion in Migrating Gray Whales, Eschrichtius Robustus. Can. J. Zoology. 61, 647–652. doi: 10.1139/z83-086

Torres, L.G., Bird, C., Rodrigues-Gonzáles, F., Christiansen F., Bejder, L., Lemos, L., Urbán Ramírez, J., Swartz, S., Willoughby, A., Hewitt., J., Bierlich, K.C. (2022). Range-wide comparison of gray whale body condition reveals contrasting sub-population health characteristics and vulnerability to environmental change. Frontiers in Marine Science. 9:867258. https://doi.org/10.3389/fmars.2022.867258

Dive into Oregon’s underwater forests

By Lisa Hildebrand, PhD student, OSU Department of Fisheries, Wildlife, & Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

When I was younger, I aspired to be a marine mammal biologist. I thought it was purely about knowing as much about marine mammal species as possible. However, over time and with experience in this field, I have realized that in order to understand a species, you need to have a holistic understanding of its prey, habitat, and environment. When I first applied to be advised by Leigh in the GEMM Lab, I had no idea how much of my time I would spend looking at tiny zooplankton under a microscope, thinking about the different benefits of different habitat types, or reading about oceanographic processes. But these things have been incredibly vital to my research to date and as a result, I now refer to myself as a marine ecologist. This holistic understanding that I am gaining will only grow throughout my PhD as I am broadly looking at the habitat use, site fidelity, and population dynamics of the Pacific Coast Feeding Group (PCFG) of gray whales for my thesis research. 

The PCFG display many foraging tactics and occupy several habitat types along the Oregon coast while they spend their summer feeding seasons here (Torres et al. 2018). Here, I will focus on one of these habitats: kelp. When you hear the word kelp, you probably conjure an image of long, thick stalks that reach from the ocean floor to the surface, with billowing fronds waving around (Figure 1a). However, this type is only one of three basic morphologies (Filbee-Dexter & Scheibling 2014) and it is called canopy kelp, which often forms extensive forests. The other two morphologies are stipitate and prostrate kelps. The former forms midwater stands (Figure 1b) while the latter forms low-lying kelp beds (Figure 1c). All three of these morphologies exist on the Oregon coast and create a mosaic of understory and canopy kelp patches that dot our coastline.

Figure 1. Examples of the three different kelp morphologies. a: bull kelp (Nereocystis luetkeana) is a type of canopy kelp and the dominant kelp on the Oregon coast (Source: Oregon Coast Aquarium); b: sea palm (Postelsia palmaeformis) is a type of stipitate kelp that forms mid-water stands (Source: Oregon Conservation Strategy); c: sea cabbage (Saccharina sessilis) is a type of prostrate kelp that is stipeless and forms low-lying kelp beds (Source: Central Coast Biodiversity).

One of the most magnificent things about kelp is that it is not just a species itself, but it provides critical habitat, refuge, and food resources to a myriad of other species due to its high rates of primary production (Dayton 1985). Kelp is often referred to as a foundation species due to all of these critical services it provides. In Oregon, many species of rockfish, which are important commercial and recreational fisheries, use kelp as habitat throughout their life cycle, including as nursery grounds. Lingcod, another widely fished species, forages amongst kelp. A large number of macroinvertebrates can be found in Oregon kelp forests, including anemones, limpets, snails, sea urchins, sea stars, and abalone, to name a fraction of them. 

Kelps grow best in cold, nutrient-rich waters (Tegner et al. 1996) and their growth and distribution patterns are highly naturally variable on both temporal and spatial scales (Krumhansl et al. 2016). However, warm water, low nutrient or light conditions, intensive grazing by herbivores, and severe storm activity can lead to the erosion and defoliation of kelp beds (Krumhansl et al. 2016). While these events can occur naturally in cyclical patterns, the frequency of several of these events has increased in recent years, as a result of climate change and anthropogenic impacts. For example, Dawn’s blog discussed increasing marine heatwaves that represent an influx of warm water for a prolonged period of time. In fact, kelps can be useful sentinels of change as they tend to be highly responsive to changes in environmental conditions (e.g., Rogers-Bennet & Catton 2019) and their nearshore, coastal location directly exposes them to human activities, such as pollution, harvesting, and fishing (Bennett et al. 2016).

Due to its foundational role, changes or impacts to kelp can reverberate throughout the ecosystem and negatively affect many other species. As mentioned previously, kelp is naturally highly variable, and like many other ecological processes, undergoes boom and bust cycles. For over four decades, dense, productive kelp forests have been shown to transition to sea urchin barrens, and back again, in natural cycles (Sala et al. 1998; Pinnegar et al. 2000; Steneck et al. 2002; Figure 2). These transitions are called phase shifts. In a healthy, balanced kelp forest, sea urchins typically passively feed on detrital plant matter, such as broken off pieces of kelp fronds that fall to the seafloor. A phase shift occurs when the grazing intensity of sea urchins increases, resulting in them actively feeding on kelp stalks and fronds to a point where the kelp in an area can become greatly reduced, creating an urchin barren. Sea urchin grazing intensity can change for a number of reasons, including reduction in sea urchin predators (e.g., sea otters, sunflower sea stars) or poor kelp recruitment events (e.g., due to warm water temperature). Regardless of the reason, the phases tend to transition back and forth over time. However, there is concern that sea urchin barrens may become an alternative stable state of the subtidal ecosystem from which kelp in an area cannot recover (Filbee-Dexter & Scheibling 2014). 

Figure 2. Screenshots from GoPro videos from 2016 (left) and 2018 (right) at the same kayak sampling station in Port Orford showing the difference between a dense kelp forest and what appears to be an urchin barren. (Source: GEMM Lab).

For example, in 2014, bull kelp canopy cover in northern California was reduced by >90% and has not shown signs of recovery since (Rogers-Bennet & Catton 2019; Figure 3). This massive decline was attributed to two major events: 1) the onset of sea star wasting disease (SSWD) in 2013 and 2) the “warm blob” of 2014-2016. SSWD affected over 20 sea star species along the coast from Mexico to Alaska, with the predatory sunflower sea star, which consumes purple sea urchins, most affected, including population declines of 80-100% along the coast (Harvell et al. 2019). Following this SSWD outbreak, the “warm blob”, which was an extreme marine heatwave in the Pacific Ocean, caused ocean temperatures to spike. These two events allowed purple sea urchin populations to grow unchecked by their predators, and created nutrient-poor and warm water conditions, which limited kelp growth and productivity. Intense grazing on bull kelp by growing urchin populations resulted in the >90% reduction in bull kelp canopy cover and has left behind widespread urchin barrens instead (Rogers-Bennet & Catton 2019). Consequently, there have been ecological and economic impacts on the ecosystem and communities in northern California. Without bull kelp, red abalone and red sea urchin populations starved, leading to a subsequent loss of the recreational red abalone (estimated value of $44 million/year) and commercial red urchin fisheries in northern California (Rogers-Bennet & Catton 2019).

Figure 3. Surface kelp canopy area pre- and post-impact from sites in Sonoma and Mendocino counties, northern California from aerial surveys (2008, 2014-2016). Figure and figure caption taken from Rogers-Bennett & Catton (2019).

As I mentioned earlier, while phase shifts between kelp forests and urchin barrens are common cycles, the intensity of the events described above in northern California are an example of sea urchin barrens potentially becoming a stable state of the subtidal ecosystem (Filbee-Dexter & Scheibling 2014). Given that marine heatwaves are only expected to increase in intensity and frequency in the future (Frölicher et al. 2018), the events documented in northern California may not be an isolated incidence. 

Considering that parts of the Oregon coast, particularly the southern portion, are very similar to northern California biogeographically, and that it was not exempt from the “warm blob”, similar changes in kelp forests may be occurring along our coast. There are many individuals and groups that are actively working on this issue to examine potential impacts to kelp and the species that depend on the services it provides. For more information, check out the Oregon Kelp Alliance

Figure 4. A gray whale surfaces in a large kelp bed during a foraging bout along the Oregon coast. (Source: GEMM Lab).

So, what does all of this information have to do with gray whales? Given their affinity for kelp habitats (Figure 4) and their zooplankton prey that aggregates there, changes to kelp ecosystems may affect gray whale health and ecology. This aspect of the complex kelp trophic web has not been examined to date; thus one of my PhD chapters focuses on the response of gray whales to changing kelp ecosystems along the southern Oregon coast. To do this, I am examining 6 years of data collected during the TOPAZ/JASPER project in Port Orford, to look at the relationships between kelp health, sea urchin density, zooplankton abundance, and gray whale foraging effort over space and time. Documenting impacts of changing kelp forests on gray whales is important to assist management efforts as healthy and abundant kelp seems critical in providing ample food opportunities for these iconic Pacific Northwest marine predators.

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References

Bennett S, et al. The ‘Great Southern Reef’: Social, ecological and economic value of Australia’s neglected kelp forests. Marine and Freshwater Research 67:47-56.

Dayton PK (1985) Ecology of kelp communities. Annual Review of Ecology and Systematics 16:215-245.

Filbee-Dexter K, Scheibling RE (2014) Sea uechin barrens as alternative stable states of collapsed kelp ecosystems. Marine Ecology Progress Series 495:1-25.

Frölicher TL, Fischer EM, Gruber N (2018) Marine heatwaves under global warming. Nature 560:360-364.

Harvell CD, et al. (2019) Disease epidemic and a marine heat wave are associated with the continental-scale collapse of a pivotal predator (Pycnopodia helianthoides). Science Advances 5(1) doi:10.1126/sciadv.aau7042.

Krumhansl KA, et al. (2016) Global patterns of kelp forest change over the past half-century. Proceedings of the National Academy of Sciences of the United States of America 113(48):13785-13790.

Pinnegar JK, et al. (2000) Trophic cascades in benthic marine ecosystems: lessons for fisheries and protected-area management. Environmental Conservation 27:179-200.

Rogers-Bennett L, Catton CA (2019) Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens. Scientific Reports 9:15050.

Sala E, Boudouresque CF, Harmelin-Vivien M (1998) Fishing, trophic cascades and the structure of algal assemblages; evaluation of an old but untested paradigm. Oikos 82:425-439.

Steneck RS, et al. (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental Conservation 29:436-459.

Tegner MJ, Dayton PK, Edwards PB, Riser KL (1996) Is there evidence for the long-term climatic change in southern California kelp forests? California Cooperative Oceanic Fisheries Investigations Report 37:111-126.

Torres LG, Nieukirk SL, Lemos L, Chandler TE (2018) Drone up! Quantifying whale behavior from a new perspective improves observational capacity. Frontiers in Marine Science doi:10.3389/fmars.2019.00319.

A pregnancy test for whales?! Why and how?

Dr. Alejandro A. Fernández Ajó, Postdoctoral Scholar, Marine Mammal Institute – OSU Department of Fisheries, Wildlife, & Conservation Sciences, Geospatial Ecology of Marine Megafauna (GEMM) Lab.

I often receive two reactions when asked what I am currently working on; one is “Wow! That is a very cool job, it must be amazing to work with such incredible animals!”, the other is “How do you do that and why is that important?”. So, today I decided to blog about some of the reasons why it is important to develop a pregnancy test for gray whales and how we are doing this.

In a previous blogpost, I described the many ways in which whales play critical roles in sustaining marine ecosystem. Briefly, whales can enhance marine productivity by vertically and horizontally mixing of ocean waters, promoting primary production, and mitigating climate change by sequestering carbon with their large biomass and long life-span (1-3). Even after they die, their carcasses can contribute to biodiversity creating new habitat on the seafloor (4). But, over several decades, the whaling industry drastically removed whales around the globe, with some species and populations depleted to near extinction (5). Consequently, these depleted whale populations now play a diminished role in ocean ecosystem processes and their recovery is currently challenged by an increasing number of modern anthropogenic impacts. Hence, working towards whale conservation is essential for keeping a healthy marine ecosystem.

Working and designing effective strategies for conservation biology often involves gaining knowledge regarding the reproductive parameters of individual animals in wild populations. This information is critical for understanding population trends and the underlaying mechanisms that affect animal welfare and their potential for recovery. However, getting such information from free-living whales can be challenging (see Hunt et al. 2013). While we know that whales typically have long life-spans, lengthy generation times, extended parental care, and high survival rates, detailed knowledge on the life history and general reproductive biology of free-ranging whales is limited for the majority of the whale populations. In fact, much of what we do know about whale reproduction is derived from whaling records. Only recently, conservation physiology approaches (see our previous post here) have contributed alternative and non-invasive methods for monitoring key physiological processes that can help monitor a whale’s reproductive biology and determine reproductive parameters such as sexual maturity and pregnancy (6-9).

In this clip you can see an example of a fecal sample collection from a gray whale off the Oregon coast. We can look at hormones in the fecal samples which are useful indicators for endocrine assessments of free-swimming whales. Fecal sample and footage filmed under NOAA/NMFS permit #16111.

Gray whales (Eschrichtius robustus) in the Eastern North Pacific (ENP) typically undertake annual migrations between their lower latitude breeding grounds in the coastal waters of the Baja California Peninsula, Mexico, and the foraging grounds located on the Bering and Chukchi Seas (10). However, among the ENP whales a distinct subgroup of about 230 whales shorten their migration to feed in the coastal waters of Northern California, Oregon, and southeastern Alaska (11). This group of whales is known as the gray whale Pacific Coast Feeding Group (PCFG).

Since 2016, the GEMM Lab has monitored individual gray whales within the PCFG off the Oregon coast (check the GRANITE project). Gray whales have a distinct mottled skin; and each individual whale presents a unique pigmentation pattern that allows for the individual identification of whales. We can identify who is who among the whales who visit the Oregon coast. In this way, we can keep a detailed record of re-sightings of known individuals (visit our new web site to know more about the lives of individual whales that visit the Oregon coast).  We have high individual re-sighting rates, so this unique opportunity helps us keep a long-term data series for individual whales to monitor their health, body condition, and reproductive status over time, and thus further develop and advance our non-invasive study methods.

We are combining behavioral and feeding ecology with drone photogrammetry and endocrinology of the same individual whales to help us understand the relationships between natural and anthropogenic drivers with biological parameters. In this way, following individual whales, we are developing sensitive biomarkers to monitor and infer about the population health, population trends, and identify stressors that impact their recovery and welfare. In particular, we are now working to develop a noninvasive approach to detect pregnancy in gray whales based on fecal hormone analyses.

In this picture you can see “Rose”, a gray whale calf, on top of her mother “Scarlett”. Scarlett is one of the most recognizable whales from the PCFG, due to a large scar on the right side of her back (not visible in this picture). She has been observed along the Pacific NW coast since 1996, so she is at least 26 years old today. We know 3 of her calves. Following individual whales like Scarlett is helping us to better understand the gray whale reproductive biology. Photo by Alejandro Fernandez Ajo taken under NOAA/NMFS permit #21678.

In marine mammals, the progesterone hormone is secreted in the ovaries during the estrous cycle and gestation, and is the predominant hormone responsible for sustaining pregnancy (12). As the hormones are cleared from the blood into the gut, they are metabolized and eventually excreted in feces; fecal samples represent a cumulative and integrated concentration of hormone metabolites (13-14), which are useful indicators for endocrine assessments of free-swimming whales. Several studies show that changes in hormone concentration correlate in meaningful ways with exposure to stressors (15-16) and changes in reproductive status (17-19). We are using our long data series of fecal hormones and individual life histories to advance our understanding on the gray whales’ reproductive biology. We are close to developing a technique that will allow us to detect pregnancy in whales based in fecal hormones analyses and photogrammetry. Stay tuned for results from this pregnancy test!

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References:

1- Pershing AJ, Christensen LB, Record NR, Sherwood GD, Stetson PB (2010) The impact of whaling on the ocean carbon cycle: Why bigger was better. PLoS ONE 5(8): e12444.

2- Roman J and McCarthy JJ. 2010. The whale pump: marine mammals enhance primary productivity in a coastal basin. PLoS ONE. 5(10): e13255.

3- Morissette L, Kaschner K, and Gerber LR. 2010. “Whales eat fish”? Demystifying the myth in the Caribbean marine ecosystem. Fish Fish 11: 388–404.

4- Smith CR, Roman J, Nation JB. A metapopulation model for whale-fall specialists: The largest whales are essential to prevent species extinctions. J. Mar. Res. 77, 283–302 (2019).

5- Branch TA, Williams TM. Legacy of industrial whaling. Whales. Whal. Ocean Ecosyst. 2006, 262–278 (2006).

6- Kellar NM, Keliher J, Trego ML, Catelani KN, Hanns C, George JC, et al. Variation of bowhead whale progesterone concentrations across demographic groups and sample matrices. Endanger Species Res 2013; 22:61–72. https://doi.org/10.3354/esr00537.

7- Pallin L, Robbins J, Kellar N, Berube M, Friedlaender A. Validation of a blubber-based endocrine pregnancy test for humpback whales. Conserv Physiol 2018;6:1 11. https://doi.org/10.1093/conphys/coy031PMID:29942518.

8-Hunt KE, Robbins J, Buck CL, Bérubé M, Rolland RM (2019) Evaluation of fecal hormones for noninvasive research on reproduction and stress in humpback whales (Megaptera novaeangliae). Gen Comp Endocrinol 280: 24–34.

9-Melica, V., Atkinson, S., Calambokidis, J., Lang, A., Scordino, J., & Mueter, F. (2021). Application of endocrine biomarkers to update information on reproductive physiology in gray whale (Eschrichtius robustus). Plos one, 16(8), e0255368.

10-Swartz SL. Gray Whale. In: Wursig B, Thewissen JGM, Kovacs KM, editors. Encyclopedia of Marine Mammals (Third Edition). Elsevier;2018,p. 422–8.https://doi.org/10.1016/B978-0-12-804327-1.00140–0.

11-Calambokidis J, Darling JD, Deecke V, Gearin P, Gosho M, Megill W, et al. Abundance, range and movements of a feeding aggregation of gray whales (Eschrichtius robustus) from California to south-eastern Alaska in 1998. J Cetacean Res Manag 2002;4:267–76.

12- Bronson, F. H. (1989). Mammalian reproductive biology. University of Chicago Press.

13-Wasser SK, Hunt KE, Brown JL, Cooper K, Crockett CM, Bechert U, Millspaugh JJ, Larson S, Monfort SL (2000) A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen Comp Endocrinol120:260–275.

14- Hunt, K.E., Rolland, R.M., Kraus, S.D., Wasser, S.K., 2006. Analysis of fecal glucocorticoids in the North Atlantic right whale (Eubalaena glacialis). Gen. Comp. Endocrinol. 148, 260–272. https://doi.org/10.1016/j.ygcen.2006.03.01215.

15- Lemos, L.S., Olsen, A., Smith, A., Burnett, J.D., Chandler, T.E., Larson, S., Hunt, K.E., Torres, L.G., 2021. Stressed and slim or relaxed and chubby? A simultaneous assessment of gray whale body condition and hormone variability. Mar. Mammal Sci. 1–11. https://doi.org/10.1111/mms.12877

16- Rolland, R., McLellan, W., Moore, M., Harms, C., Burgess, E., Hunt, K., 2017. Fecal glucocorticoids and anthropogenic injury and mortality in North Atlantic right whales Eubalaena glacialis. Endanger. Species Res. 34, 417–429. https://doi.org/10.3354/esr00866.

17-Rolland, R.M., Hunt, K.E., Kraus, S.D., Wasser, S.K., 2005. Assessing reproductive status of right whales (Eubalaena glacialis) using fecal hormone metabolites. Gen. Comp. Endocrinol. 142, 308–317. https://doi.org/10.1016/j.ygcen.2005.02.002

18- Valenzuela Molina M, Atkinson S, Mashburn K, Gendron D, Brownell RL. Fecal steroid hormones reveal reproductive state in female blue whales sampled in the Gulf of California, Mexico. Gen Comp Endocrinol 2018;261:127–35.https://doi.org/10.1016/j.ygcen.2018.02.015 PMID:29476760.

19- Hunt, K. E., Robbins, J., Buck, C. L., Bérubé, M., & Rolland, R. M. (2019). Evaluation of fecal hormones for noninvasive research on reproduction and stress in humpback whales (Megaptera novaeangliae). General and Comparative Endocrinology, 280, 24-34.