Fantastic beasts and how to measure  them! 

Sagar Karki, Master’s student in the Computer Science Department at Oregon State University 

What beasts? Good question! We are talking about gray whales in this article but honestly we can tweak the system discussed in this blog a little and make it usable for other marine animals too.  

Understanding the morphology, such as body area and length, of wild animals and populations can provide important information on animal  behavior and health (check out postdoc Dr. KC Bierlich’s post on this topic). Since 2015, the GEMM Lab has been flying drones over whales to collect aerial imagery to allow for photogrammetric measurements to gain this important morphological data. This photogrammetry data has shed light on multiple important aspects of gray whale morphology, including the facts that the whales feeding off Oregon are skinnier [1] and shorter [2] than the gray whales that feed in the Arctic region.  But, these surprising conclusions overshadow the immense, time-consuming labor that takes place behind the scenes to move from aerial images to accurate measurements.  

To give you a sense of this laborious process, here is a quick run through of the methods: First the 10 to 15 minute videos must be carefully watched to select the perfect frames of a whale (flat and straight at the surface) for measurement. The selected frames from the drone imagery are then imported into MorphoMetriX, which is a custom software developed for photogrammetry measurement [1]. MorphoMetriX is an interactive application that allows an analyst to manually measure the length by clicking points along the centerline of the whale’s body. Based on this line, the whale is divided into a set of sections perpendicular to the centerline, these are used to then measure widths along the body. The analyst then clicks border points at the edge of the whale’s body to delineate the widths following the whale’s body curve. MorphoMetriX then generates a file containing the lengths and widths of the whale in pixels for each measured image. The length and widths of whales are converted from pixels to metric units using a software called CollatriX [4] and this software also calculates metrics of body condition from the length and width measurements. 

While MorphoMetriX [3] and CollatriX [4] are both excellent platforms to facilitate these photogrammetry measurements, each measurement takes time, a keen eye, and attention to detail. Plus, if you mess up one step, such as an incorrect length or width measurement, you have to start from the first step. This process is a bottleneck in the process of obtaining important morphology data on animals. Can we speed this process up and still obtain reliable data? 

What if we can apply automation using computer vision to extract the frames we need and automatically obtain measurements that are as accurate as humans can obtain? Sounds pretty nice, huh? This is where I come into the picture. I am a Master’s student in the Computer Science Department at OSU, so I lack a solid background in marine science, but bring to the table my skills as a computer programmer. For my master’s project, I have been working in the GEMM Lab for the past year to develop automated methods to obtain accurate photogrammetry measurements of whales.  

We are not the first group to attempt to use computers and AI to speed up and improve the identification and detection of whales and dolphins in imagery. Researchers have used deep learning networks to speed up the time-intensive and precise process of photo-identification of  individual whales and dolphins [5], allowing us to more quickly determine animal location, movements and abundance. Millions of satellite images of the earth’s surface are collected daily and scientists are attempting to utilize these images to  benefit marine life by studying patterns of species occurrence, including detection of gray whales in satellite images using deep learning [6]. There has also been success using computer vision to identify whale species and segment out the body area of the whales  from drone imagery [7]. This process involves extracting segmentation masks of the whale’s body followed by length extraction from the mask. All this previous research shows promise for the application of computer vision and AI to assist with animal research and conservation. As discussed earlier, the automation of image extraction and photogrammetric measurement  from drone videos will help researchers collect vital data more quickly so that decisions that impact  the health of whales can be more responsive and effective.For instance,  photogrammetry data extracted from drone images can diagnose pregnancy of the whales [8], thus automation of this information could speed up our ability to understand population trends. 

Computer vision and natural language processing fields are growing exponentially. There are new foundation models like ChatGPT that can do most of the natural language understanding and processing tasks. Foundational models are also emerging for computer vision tasks, such as “the segment anything model” from Meta. Using these foundation models along with other existing research work in computer vision, we have developed and deployed a system that automates the manual and computational tasks of MorphoMetriX and CollatriX systems.  

This system is currently in its testing and monitoring phase, but we are rapidly moving toward a publication to disseminate all the tools developed, so stay tuned for the research paper that will explain in detail the methodologies followed on data processing, model training and test results. The following images give a sneak peak of results. Each image  illustrates a frame from a drone video that was  identified and extracted through automation, followed by another automation process that identified important points along the whale’s body and curvature.  The user interface of the system aims to make the user experience intuitive and easy to follow. The deployment is carefully designed to run on different hardwares, with easy monitoring and update options using the latest open source frameworks. The user has to do just two things. First, select the videos for analysis. The system then generates potential frames for photogrammetric analysis (you don’t need to watch 15 mins of drone footage!). Second, the user selects the frame of choice for photogrammetric analysis and waits for the system to give you measurements. Simple! Our goal is for these softwares to be a massive time-saver while  still providing vital, accurate body measurements  to the researchers in record time. Furthermore, an advantage of this approach is that researchers can follow the methods in our to-be-soon-published research paper to make  a few adjustments enabling the software to measure other marine species, thus expanding the impact of this work to many other life forms.  

Did you enjoy this blog? Want to learn more about marine life, research, and conservation? Subscribe to our blog and get a weekly message when we post a new blog. Just add your name and email into the subscribe box below.

Loading

References 

  1. Torres LG, Bird CN, Rodríguez-González F, Christiansen F, Bejder L, Lemos L, Urban R J, Swartz S, Willoughby A, Hewitt J, Bierlich K (2022) Range-Wide Comparison of Gray Whale Body Condition Reveals Contrasting Sub-Population Health Characteristics and Vulnerability to Environmental Change. Front Mar Sci 910.3389/fmars.2022.867258 
  1. Bierlich KC, Kane A, Hildebrand L, Bird CN, Fernandez Ajo A, Stewart JD, Hewitt J, Hildebrand I, Sumich J, Torres LG (2023) Downsized: gray whales using an alternative foraging ground have smaller morphology. Biol Letters 19:20230043 doi:10.1098/rsbl.2023.0043 
  1. Torres et al., (2020). MorphoMetriX: a photogrammetric measurement GUI for morphometric analysis of megafauna. Journal of Open Source Software, 5(45), 1825, https://doi.org/10.21105/joss.01825 
  1. Bird et al., (2020). CollatriX: A GUI to collate MorphoMetriX outputs. Journal of Open Source Software, 5(51), 2328, https://doi.org/10.21105/joss.02328 
  1. Patton, P. T., Cheeseman, T., Abe, K., Yamaguchi, T., Reade, W., Southerland, K., Howard, A., Oleson, E. M., Allen, J. B., Ashe, E., Athayde, A., Baird, R. W., Basran, C., Cabrera, E., Calambokidis, J., Cardoso, J., Carroll, E. L., Cesario, A., Cheney, B. J. … Bejder, L. (2023). A deep learning approach to photo–identification demonstrates high performance on two dozen cetacean species. Methods in Ecology and Evolution, 00, 1–15. https://doi.org/10.1111/2041-210X.14167 
  1. Green, K.M., Virdee, M.K., Cubaynes, H.C., Aviles-Rivero, A.I., Fretwell, P.T., Gray, P.C., Johnston, D.W., Schönlieb, C.-B., Torres, L.G. and Jackson, J.A. (2023), Gray whale detection in satellite imagery using deep learning. Remote Sens Ecol Conserv. https://doi.org/10.1002/rse2.352 
  1. Gray, PC, Bierlich, KC, Mantell, SA, Friedlaender, AS, Goldbogen, JA, Johnston, DW. Drones and convolutional neural networks facilitate automated and accurate cetacean species identification and photogrammetry. Methods Ecol Evol. 2019; 10: 1490–1500. https://doi.org/10.1111/2041-210X.13246 
  1. Fernandez Ajó A, Pirotta E, Bierlich KC, Hildebrand L, Bird CN, Hunt KE, Buck CL, New L, Dillon D, Torres LG (2023) Assessment of a non-invasive approach to pregnancy diagnosis in gray whales through drone-based photogrammetry and faecal hormone analysis. Royal Society Open Science 10:230452 

That’s so Real: Adult Beginners, Serial Podcast(s), and a whole lotta of Baja Gray Whale Video Analysis.

Celest Sorrentino, Research Technician, Geospatial Ecology of Marine Megafauna Lab

Hello again GEMM Lab family. I write to you exactly a year after (okay maybe 361 days after but who’s counting…) from my previous blog post describing my 2022 summer working in the GEMM Lab as an NSF REU intern. Since then, so much has changed, and I can’t wait to fill you in on it.

In June I walked across the commencement stage at UC Santa Barbara, earning my BS in Ecology, Evolution, and Marine Biology and my minor in Italian language. A week later, I packed my bags and headed straight back to the lukewarm beaches of Newport, Oregon as a Research Technician in the GEMM Lab. I am incredibly fortunate to have been invited back to the OSU Marine Mammal Institute to lend a hand analyzing drone footage of gray whales collected back in March 2023 when Leigh and Clara went down to Baja California, as mentioned previously in Clara’s blog

Fig. 1. View from the top! (of the bridge at Yaquina Bay Bridge in Newport, OR)

During my first meeting with Clara at the beginning of the summer we discussed that a primary goal of my position was to process all the drone footage collected in Baja so that the generated video clips could be later used in other analytical software such as BORIS and SLEAP A.I. Given my previous internships and past summer project, this video processing is familiar to me. My initial thoughts were:

Sweet! Watch drone footage, pop in some podcasts, note down when I see whales, let’s do this!*

Like any overly eager 23-year-old, I might have mentally cracked open a Celsius and kicked my feet up too soon. We added another layer to the goal: develop an ethogram – which requires me to identify and define the behaviors that the gray whales appear to be demonstrating within the videos (more on ethogram development in Clara’s previous blog.) This made me nervous. 

I don’t have any experience with behavior. How do I tell what is a real behavior or if the whale is just existing? What if I’m wrong and ruin the project? What if I totally mess this up?

Naturally, as any sane person, to resolve these thoughts I took to the Reddit search bar: “How to do a job you’ve never done before.” No dice. 

I pushed these thoughts aside and decided to just start the video analysis process. Clara provided me with the ethogram she is developing during her PhD as a point of reference (based on the published gray whale ethogram in Torres et al. 2018), I was surrounded by an insanely supportive lab, and I could Google anything at my fingertips. Fast-forward 6 weeks later: I had analyzed 128 drone videos of adult gray whales as well as mother-calf pairs, and developed an ethogram describing, 26 behaviors**. I named one of my favorite behaviors  a “Twirl” to describe when a gray whale lifts their head out of the water and performs a 360 turn. Reminds me of times when as a kid, sometimes all you really needed is a good spin!

Now I was ready to start a productive, open conversation with Leigh and Clara about this ethogram and my work. However, even walking up to that last meeting, remnants of those daunting, doubtful early summer thoughts persisted. Even after I double checked all the definitions I wrote, rewatched all videos with said behaviors, and had something to show for my work. What gives Brain?

A few days ago, as I sat on my family’s living room couch with my two younger sisters, Baylie and Cassey, Baylie wanted to watch some TikToks with me. One video that came up was of a group of adults taking a beginner dance class, having so much fun and radiating joy. The caption read, Being a beginner as an adult is such a fun and wild thing. Baylie and I watched the video at least 10x, repeating to each other phrases like, “Wow!” and “They’re so cool.” That caption and video has been on my mind since: 

Being a beginner as an adult is such a fun and wild thing.

Being a beginner as an adult is also scary. 

Having just graduated, I can no longer say I am undergraduate student. Now, I am a young adult. This was my first research technician job, as an adult. Don’t adults usually have everything figured out? Can adults be beginners too?

Yes. In fact, we’re beginners more than we realize. 

  • I was a beginner cooking my mother’s turkey recipe 3 years ago for my housemates during the pandemic (Even after having her on Facetime, I still managed to broil it a little too long.) 
  • I was a beginner driver 5 years ago in a rickety Jeep driving myself to school (Now, since I’ve been back home, I’ve been driving my little sisters to school.)
  • I was a beginner NSF REU intern just a year ago. (This summer I was the alumni on the panel for the current NSF REU interns at Hatfield.)
  • I was a beginner science communicator presenting my NSF REU project at Hatfield last summer. (This summer, I presented my research at the Animal Behavior Society Conference.) 
Fig 2A. Group Pic with the LABIRINTO Lab and GEMM Lab at the ABS Portland Conference!
Fig 2B. Clara Bird (left), Dr. Leigh Torres (middle), and I (right) at the ABS Portland Conference. 

I now recognize that during my time identifying and defining behaviors of gray whales in videos made me take on the seat of a “beginner video and behavioral analyst”. I could not rely on the automated computer vision lens I gained from previous internships, which felt familiar and secure. 

 Instead, I had to allow myself to be creative. Dig into the unfamiliar in an effort to complete a task or job I had never done before. Allowing myself to be imperfect, make mistakes, meanwhile unconsciously building a new skill. 

This is what makes being a beginner as an adult such a fun thing. 

I don’t think being a beginner is a wild thing, although it can definitely make you feel a wild range of emotions. Being a beginner means you’re allowing yourself to try something new. Being a beginner means you’re allowing yourself the chance to learn.

Whether you’re an adult beginner as you enter your 30s, adult beginner as you enter parenthood, adult beginner grabbing a drink with friends after a long day in lab, adult beginner as a dancer, or like me, a beginner of leaving behind my college student persona and entering a new identity of adulthood, being a beginner as an adult is such a fun and normal thing.

I am not sure what will be next, but I hope to write to you all again from this blog a year from now, as an adult beginner as a grad student in the GEMM Lab. For anyone approaching the question of “What’s next”, I encourage you to read “Never a straight Path” by GEMM Lab MSc alum Florence Sullivan, a blog that has brought me such solace in my new adult journey and advice that never gets old.

Being a beginner—that, is so real. 

Fig 3A. Kayaking as an adult beginner of the Port Orford Field Team!
Fig 3B “See you soon:” Wolftree evenings with the lab.
Fig 3C. GEMM Lab first BeReal!

*I listened to way too many podcasts to list them all, but I will include two that have been a GEMM Lab “gem” —-thanks to Lisa and Clara for looping me in and now, looping you in!)

**(subject to change)

References

Torres LG, Nieukirk SL, Lemos L, Chandler TE (2018) Drone Up! Quantifying Whale Behavior From a New Perspective Improves Observational Capacity. Front Mar Sci 510.3389/fmars.2018.00319

Did you enjoy this blog? Want to learn more about marine life, research, and conservation? Subscribe to our blog and get a weekly message when we post a new blog. Just add your name and email into the subscribe box below.

Loading

Individual Specialization Part 3: How do individual characteristics relate to individual specialization?

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

While I did not mean to start a mini-blog series on individual specialization, here I am with my third blog about individual specialization in as many years. Looking back, these blogs are actually a lovely documentation of my own journey of learning about individual specialization and I hope you’re enjoying being along for the ride.

So, what have we learned so far? In my first blog I described the concept of individual specialization, why it matters, and presented some case studies. In my second blog I discussed the roles of competition and learning as drivers of individual specialization. Let’s review: Individual specialization is when individuals within a population only use a subset of the resources that the full population uses, but different individuals use different subsets. This is important to quantify for two reasons: (1) it affects how we think about conserving and managing a population (Bolnick et al., 2003), and (2) it can affect the relationships between the population and the other species in its community (Bolnick et al., 2011). Common drivers of specialization are competition and learning. Competition can lead to specialization because it reduces the availability of a resource, driving individuals to switch resource use (Pianka, 1974). Learning can also lead to specialization through ‘one-to-one’ learning, where one individual learns from one demonstrator (Sheppard et al., 2018). This individual tends to then use, and eventually teach, that specialized technique.

While understanding these drivers is important, the question of why specific individuals employ specific specializations remains. If learning is not the driver of specialization, then how do individuals end up using their specific subset. Is it random? Or are there underlying patterns? The common sources of variation are related to sex, age, or size (and often these three can be inter-connected) (Dall et al., 2012). 

Individual differences related to the sex of the individuals are called sexual dimorphisms. Physical and ecological differences between the sexes are common throughout nature (peacocks for example) and these differences can lead to different specializations. Northern elephant seals provide a fascinating example (Kienle et al., 2022). Northern elephant seal males are the distinctly larger sex as they engage in competitionfor females. Because of their larger body size and energy expenditure during competition, they have much higher energetic requirements than females during the breeding season, meaning that they need to consume more prey. This elevated requirement has led to a difference in foraging behaviors. Males forage near the continental shelf where there is more prey while females forage further offshore in the open ocean. However, the tradeoff of feeding on the continental shelf is an increased predation risk due to overlap with predator habitat, and indeed Kienle et al. found that the mortality rate for foraging trips was 5-6 times higher for males than females. So, while males need to take the risk of foraging in an area with higher predator presence to meet their energetic demands, females can forage in a safer habitat with less prey because their energetic requirements are lower. This study presents an excellent example of how sexual dimorphism can cause individual specialization and the subsequent consequences.

An illustration depicting a male (background) and female (foreground) northern elephant seal. source: https://www.sciencedirect.com/topics/agricultural-and-biological-sciences/northern-elephant-seal. Illustration by Pieter Folken.

Individual specializations attributed to differences between distinct morphs are called resource polymorphisms. A morph is the physical appearance of an individual; distinct morphs are when there are clearly different kinds of morphs within a population. Morphs can range from color polymorphism (ex. lizards of different colors within the same species) to differences in skull shape and size. A study on the European eel found that differences in skull morphology were related to different foraging strategies (Cucherousset et al., 2011).  Eels with larger head widths consumed larger prey types. Interestingly, they found that eels on either end of the head width spectrum (i.e., very narrow or very wide) were more successful (i.e., in better body condition) than eels with intermediate head widths. They suggest that this difference in nutrition success is because the intermediate head width eels were less efficient foragers than eels at the extremes. In this example we see that morphology is related to the ability to feed on a prey type and has consequences for individual health.

Figure 2. from Cucherousset et al., 2011. Small-bodied eels with narrower (a) and broader (b) heads and large-bodied eels with narrower (c) and broader (d) heads. TL (Total Length) and HW (Head Width):TL are shown for each individual

Individual differences related to changes in size, shape, and behavior that occur as an individual grows are called ontogenetic shifts. As you have experienced yourself, there are many changes that occur as an individual grows, and these changes can mean that different age classes have different specializations. Gustafsson (1988) found an ontogenetic shift in where coal tits (a species of bird) fed within a pine tree. Younger birds were more generalists but tended to feed on the outer sections of the tree, while adults foraged on the more profitable, central portion of the tree. He attributes this difference to dominance of adults over juveniles. Gustafsson also found that the larger individuals within each age class also tended to feed closer to the center of the tree. This within age class difference is attributed to a larger body size being better suited for feeding closer to the center of the tree, while smaller body sizes are better suited for hovering and foraging on the outside. Interestingly, this study occurred over multiple years, and Gustafsson documented several juvenile individuals that shifted foraging behavior when they became adults. 

Photo of a coal tit. Source: https://ebird.org/species/coatit2

These sources of behavioral variation are important to account for because ultimately phenotypic variation can affect not only a population’s niche, but its population size, distribution, evolutionary potential, and vulnerability to environmental change (Wennersten & Forsman, 2012). And it’s important to determine which source(s) of variation are at play to inform best population management practices. Different behaviors between sexes versus age classes have different implications for the population, making it necessary to not only assess if there are differences but also to try and understand their drivers.

This behavioral variability relative to morphs is something that is of particular interest to me, and it is the focus of my first chapter. We’ve documented that the PCFG gray whales in our study region employ a variety of foraging tactics, and I want to know if there is specialization in tactic use and if we can find an underlying source of the variation. I can’t wait to share results with you in the next installment of this individual specialization journey. Stay tuned!

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 below!

Loading

References

Bolnick, D. I., Amarasekare, P., Araújo, M. S., Bürger, R., Levine, J. M., Novak, M., Rudolf, V. H. W., Schreiber, S. J., Urban, M. C., & Vasseur, D. A. (2011). Why intraspecific trait variation matters in community ecology. Trends in Ecology & Evolution26(4), 183–192. https://doi.org/10.1016/j.tree.2011.01.009

Bolnick, D. I., Svanbäck, R., Fordyce, J. A., Yang, L. H., Davis, J. M., Hulsey, C. D., & Forister, M. L. (2003). The ecology of individuals: Incidence and implications of individual specialization. American Naturalist161(1), 1–28. https://doi.org/10.1086/343878

Cucherousset, J., Acou, A., Blanchet, S., Britton, J. R., Beaumont, W. R. C., & Gozlan, R. E. (2011). Fitness consequences of individual specialisation in resource use and trophic morphology in European eels. Oecologia167(1), 75–84. https://doi.org/10.1007/s00442-011-1974-4

Dall, S. R. X., Bell, A. M., Bolnick, D. I., & Ratnieks, F. L. W. (2012). An evolutionary ecology of individual differences. Ecology Letters15(10), 1189–1198. https://doi.org/10.1111/j.1461-0248.2012.01846.x

De Meyer, J., Belpaire, C., Boeckx, P., Bervoets, L., Covaci, A., Malarvannan, G., De Kegel, B., & Adriaens, D. (2018). Head shape disparity impacts pollutant accumulation in European eel. Environmental Pollution240, 378–386. https://doi.org/10.1016/j.envpol.2018.04.128

Gustafsson, L. (1988). Foraging behaviour of individual coal tits, Parus ater, in relation to their age, sex and morphology. Animal Behaviour36(3), 696–704. https://doi.org/10.1016/S0003-3472(88)80152-0

Kienle, S. S., Friedlaender, A. S., Crocker, D. E., Mehta, R. S., & Costa, D. P. (2022). Trade-offs between foraging reward and mortality risk drive sex-specific foraging strategies in sexually dimorphic northern elephant seals. Royal Society Open Science9(1), 210522. https://doi.org/10.1098/rsos.210522

Pianka, E. R. (1974). Niche Overlap and Diffuse Competition71(5), 2141–2145.

Sheppard, C. E., Inger, R., McDonald, R. A., Barker, S., Jackson, A. L., Thompson, F. J., Vitikainen, E. I. K., Cant, M. A., & Marshall, H. H. (2018). Intragroup competition predicts individual foraging specialisation in a group-living mammal. Ecology Letters21(5), 665–673. https://doi.org/10.1111/ele.12933

Wennersten, L., & Forsman, A. (2012). Population-level consequences of polymorphism, plasticity and randomized phenotype switching: A review of predictions. Biological Reviews87(3), 756–767. https://doi.org/10.1111/j.1469-185X.2012.00231.x

A Gut Feeling: DNA Metabarcoding Gray Whale Diets

By Charles Nye, graduate student, OSU Department of Fisheries, Wildlife, & Conservation Sciences, Cetacean Conservation and Genomics Laboratory

Figure 1: An illustration (by me) of a feeding gray whale whose caudal end transitions into a DNA double helix.

Let’s consider how much stuff organisms shed daily. If you walk down a hallway, you’ll leave a microscopic trail of skin cells, evaporated sweat, and even more material if you so happen to sneeze or cough (as we’ve all learned). The residency of these bits and pieces in a given environment is on the order of days, give or take (Collins et al. 2018). These days, we can extract, amplify, and sequence DNA from leftover organismal material in environments (environmental DNA; eDNA), stomach contents (dietary DNA, dDNA), and other sources (Sousa et al. 2019; Chavez et al. 2021).

You might be familiar with genetic barcoding, where scientists are able to use documented and annotated pieces of a genome to identify a piece of DNA down to a species. Think of these as genetic fingerprints from a crime scene where all (described) species on Earth are prime suspects. With advancements in computing technology, we can barcode many species at the same time—a process known as metabarcoding. In short, you can now do an ecosystem-wide biodiversity survey without even needing to see your species of interest (Ficetola et al. 2008; Chavez et al. 2021).

(Before you ask: yes, people have tried sampling Loch Ness and came up with not a single strand of plesiosaur DNA (University of Otago, 2019).)

I received my crash course on metabarcoding when I was employed at the Monterey Bay Aquarium Research Institute (MBARI), right before grad school. There, I was employed to help refine eDNA survey field and laboratory methods (in addition to some cool robot stuff). Here at OSU, I use metabarcoding to research whale ecology, detection, and even a little bit of forensics  work. Cetacean species (or evidence thereof) I’ve worked on include North Atlantic right whales (Eubalaena glacialis), killer whales (Orcinus spp.), and gray whales (Eschrichtius robustus).

Long-time readers of the GEMM Lab Blog are probably quite knowledgeable about the summertime grays—the Pacific Coast Feeding Group (PCFG). All of us here at OSU’s Marine Mammal Institute (MMI) are keenly interested in understanding why these whales hang out in the Pacific Northwest during the summer months and what sets them apart from the rest of the Eastern North Pacific gray whale population. What interests me? Well, I want to double-check what they’re eating—genetically.

“What does my study species eat?” is a straightforward but underappreciated question. It’s also deceptively difficult to address. What if your species live somewhere remote or relatively inaccessible? You can imagine this is a common logistical issue for most research in marine sciences. How many observations do you need to make to account for seasonal or annual changes in prey availability? Do all individuals in your study population eat the same thing? I certainly like to mix and match my diet.

Gray whale foraging ecology has been studied comprehensively over the last several decades, including an in-depth stomach content evaluation by Mary Nerini in 1984 and GEMMer Lisa Hildebrand’s MSc research. PCFG whales seem to prefer shrimpy little creatures called mysids, along with Dungeness crab (Cancer magister) larvae, during their stay in the Pacific Northwest (PNW), most notably the mysid Neomysis rayii (Guerrero 1989; Hildebrand et al. 2021). Indeed, the average energetic values of common suspected prey species in PNW waters rival the caloric richness of Arctic amphipods (Hildebrand et al. 2021). However, despite our wealth of visual foraging observations, metabarcoding may add an additional layer of resolution. For example, the ocean sunfish (Mola mola) was believed to exclusively forage on gelatinous zooplankton, but a metabarcoding approach revealed a much higher diversity of prey items, including other bony fishes and arthropods (Sousa et al. 2016).

Given all this exposition, you may be wondering: “Charles—how do you intend on getting dDNA from gray whales? Are you going to cut them open?”

Figure 2: The battle station, a vacuum pump that I use to filter out all of the particulate matter from a gray whale dDNA sample. The filter is made of polycarbonate track etch material, which melts away in the DNA extraction process—quite handy, indeed!

No. I’m going to extract DNA from their poop.

Well, actually, I’ve been doing that for the last two years. My lab (Cetacean Conservation and Genomics Laboratory, CCGL) and GEMM Lab have been collaborating to make lemonade out of, er…whale poop. An archive of gray whale fecal samples (with ongoing collections every field season) originally collected for hormone analyses presented itself with new life—the genomics kind. In addition to community-level data, we are also able to recover informative DNA from the gray whales, including sex ID from “depositing” individuals, though the recovery rate isn’t perfect.

Because the GEMM Lab/MMI can non-invasively collect multiple samples from the same individuals over time, dDNA metabarcoding is a great way to repeatedly evaluate the diets of the PCFG, just shy of being at the right place at the right time with a GoPro or drone to witness a feeding event.  While we can get stomach contents and even usable dDNA from a naturally deceased whale, those data may not be ideal. How representative a stranded whale is of the population is dependent on the cause of death; an emaciated or critically injured individual, for example, is a strong outlier.

Figure 3: Presence/absence of the top 10 most-common taxonomic Families observed in the PCFG gray whale dDNA dataset (n = 20, randomly selected). Filled-in dots indicate at least one genetic read associated with that Family, and empty dots indicate none. Note the prey taxa: mysids (Mysidae), krill (Euphausiidae), and olive snails (Olividae).

Here’s a snapshot of progress to date for this dDNA metabarcoding project. I pulled out twenty random samples from my much larger working dataset (n = 82) for illustrative purposes (and legibility). After some bioinformatic wizardry, we can use a presence/absence approach to get an empirical glimpse at what passes through a PCFG gray whale. While I am able to recover species-level information, using higher-level taxonomic rankings summarizes the dataset in a cleaner fashion (and also, not every identifiable sequence resolves to species).

The title of most commonly observed prey taxa belongs to our friends, the mysids (Mysidae). Surprisingly, crabs and amphipods are not as common in this dataset, instead losing to krill (Euphausiidae) and olive snails (Olividae). The latter has been found in association with gray whale foraging grounds but not documented in a prey study (Jenkinson 2001). We also get an appreciable amount of interference from non-prey taxa, most notably barnacles (Balanidae), with an honorable mention to hydrozoans (Clytiidae, Corynidae). While easy to dismiss as background environmental DNA, as gray whales do forage at the benthos, these taxa were physically present and identifiable in Nerini’s (1984) gray whale stomach content evaluation.

So—can we conclude that barnacles and hydrozoans are an important part of a gray whale’s diet, as much as mysids? From decades of previous observations, we might say…probably not. Gray whales are actively targeting patches of crabby, shrimpy zooplankton things, and even employ novel foraging strategies to do so (Newell & Cowles 2006; Torres et al. 2018). However, the sheer diversity of consumed species does present additional dimensionality to our understanding of gray whale ecology.

The whales are eating these ancillary organisms, whether they intend to or not, and this probably does influence population dynamics, recruitment, and succession in these nearshore benthic habitats. After all, the shallow pits that gray whales leave behind post-feeding provide a commensal trophic link with other predatory taxa, including seabirds and groundfish (Oliver & Slattery 1985). Perhaps the consumption of these collateral species affects gray whale energetics and reflects on their “performance”?

I hope to address all of this and more in some capacity with my published work and graduate chapters. I’m confident to declare that we can document diet composition of PCFG whales using dDNA metabarcoding, but what comes next is where one can get lost in the sea(weeds). How does the diet of individuals compare to one another? What about at differing time points? Age groups? How many calories are in a barnacle? No need to fret—this is where the fun begins!

References

Chavez F, Min M, Pitz K, Truelove N, Baker J, LaScala-Grunewald D, Blum M, Walz K,

Nye C, Djurhuus A, et al. 2021. Observing Life in the Sea Using Environmental

DNA Oceanog. 34(2):102–119. doi:10.5670/oceanog.2021.218.

Collins R, Wangensteen OS, O’Gorman EJ, Mariani S, Sims DW, Genner M. 2018. Persistence

of environmental DNA in marine systems. Comm Biol. 1(185).

https://doi.org/10.1038/s42003-018-0192-6

Ficetola GF, Miaud C, Pompanon F, Taberlet P. 2008. Species detection using

environmental DNA from water samples. Biol Lett. 4(4):423–425.

doi:10.1098/rsbl.2008.0118.

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. 8:683634.

doi:10.3389/fmars.2021.683634.

Jenkinson R. 2001. Gray whale (Eschrichtius robustus) prey availability and feeding ecology in

northern California, 1999-2000 [thesis]. California State Polytechnic University,

Humboldt. 81 p.

Newell CL, Cowles TJ. 2006. Unusual gray whale Eschrichtius robustus feeding in the summer

of 2005 off the central Oregon Coast. Geophys Res Lett. 33(22):L22S11.

doi:10.1029/2006GL027189.

Oliver JS, Slattery PN. 1985. Destruction and Opportunity on the Sea Floor: Effects of

Gray Whale Feeding. Ecology. 66(6):1965–1975. doi:10.2307/2937392.

Sousa LL, Silva SM, Xavier R. 2019. DNA metabarcoding in diet studies: Unveiling

ecological aspects in aquatic and terrestrial ecosystems. Environmental DNA.

1(3):199–214. doi:10.1002/edn3.27.

Sousa LL, Xavier R, Costa V, Humphries NE, Trueman C, Rosa R, Sims DW, Queiroz N.

2016. DNA barcoding identifies a cosmopolitan diet in the ocean sunfish. Sci

Rep. 6(1):28762. doi:10.1038/srep28762.

Torres LG, Nieukirk SL, Lemos L, Chandler TE. 2018. Drone Up! Quantifying Whale Behavior

From a New Perspective Improves Observational Capacity. Front Mar Sci. 5:319.

doi:10.3389/fmars.2018.00319.

University of Otago. 2019. First eDNA study of Loch Ness points to something fishy.

https://www.otago.ac.nz/news/news/otago717609.html. [accessed 2023 Apr 25]

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!

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 below!

Loading

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!

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 below!

Loading

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

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. 

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 below!

Loading

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!

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

[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.