The costs and benefits of automated behavior classification

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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References

Anderson, D. J., & Perona, P. (2014). Toward a Science of Computational Ethology. Neuron84(1), 18–31. https://doi.org/10.1016/j.neuron.2014.09.005

Bozek, K., Hebert, L., Portugal, Y., Mikheyev, A. S., & Stephens, G. J. (2021). Markerless tracking of an entire honey bee colony. Nature Communications12(1), 1733. https://doi.org/10.1038/s41467-021-21769-1

Ebbesen, C. L., & Froemke, R. C. (2021). Body language signals for rodent social communication. Current Opinion in Neurobiology68, 91–106. https://doi.org/10.1016/j.conb.2021.01.008

Mayo, C. A., & Marx, M. K. (1990). Surface foraging behaviour of the North Atlantic right whale, Eubalaena glacialis , and associated zooplankton characteristics. Canadian Journal of Zoology68(10), 2214–2220. https://doi.org/10.1139/z90-308

Mearns, D. S., Donovan, J. C., Fernandes, A. M., Semmelhack, J. L., & Baier, H. (2020). Deconstructing Hunting Behavior Reveals a Tightly Coupled Stimulus-Response Loop. Current Biology30(1), 54-69.e9. https://doi.org/10.1016/j.cub.2019.11.022

Nielsen, M., Sprogis, K., Bejder, L., Madsen, P., & Christiansen, F. (2019). Behavioural development in southern right whale calves. Marine Ecology Progress Series629, 219–234. https://doi.org/10.3354/meps13125

Pereira, T. D., Shaevitz, J. W., & Murthy, M. (2020). Quantifying behavior to understand the brain. Nature Neuroscience23(12), 1537–1549. https://doi.org/10.1038/s41593-020-00734-z

Little whale, big whale, swimming in the water: A quick history on how aerial photogrammetry has revolutionized the ability to obtain non-invasive measurements of whales

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

The morphology and body size of an animal is one of the most fundamental factors for understanding a species ecology. For instance, fish body size and fin shape can influence its habitat use, foraging behavior, prey type, physiological performance, and predator avoidance strategies (Fig 1). Morphology and body size can thus reflect details of an individual’s current health, likelihood of survival, and potential reproductive success, which directly influences a species life history patterns, such as reproductive status, growth rate, and energetic requirements. Collecting accurate morphological measurements of individuals is often essential for monitoring populations, and recent studies have demonstrated how animal morphology has profound implications for conservation and management decisions, especially for populations inhabiting anthropogenically-altered environments (Miles 2020) (Fig. 1). For example, in a study on the critically endangered European eel, De Meyer et al. (2020) found that different skulls sizes were associated with different ecomorphs (a local variety of a species whose appearance is determined by its ecological environment), which predicted different diet types and resulted with some ecomorphs having a greater exposure to pollutants and toxins than others. However, obtaining manual measurements of wild animal populations can be logistically challenging, limited by accessibility, cost, danger, and animal disturbance. These challenges are especially true for large elusive animals, such as whales that are often in remote locations, spend little time at the surface of the water, and their large size can preclude safe capture and live handling.

Figure 1. Top) A pathway framework depicting how the morphology of an animal influences its habitat use, behavior, foraging, physiology, and performance. These traits all affect how successful an animal is in its environment and can reflect an individual’s current health, likelihood of survival, and potential reproductive success. This individual success can then be scaled up to assess overall population health, which in turn can have direct implications for conservation. Bottom) an example of morphological differences in fish body size and fin shape from Walker et al. (2013). Fineness ratio (f) = length of body ­÷ max body width. 

Photogrammetry is a non-invasive method for obtaining accurate morphological measurements of animals from photographs. The two main types of photogrammetry methods used in wildlife biology are 1) single camera photogrammetry, where a known scale factor is applied to a single image to measure 2D distances and angles and 2) stereo-photogrammetry, where two or more images (from a single or multiple cameras) are used to recreate 3D models. These techniques have been used on domestic animals to measure body condition and estimate weight of dairy cows and lactating Mediterranean buffaloes (Negretti et al., 2008; Gaudioso et al., 2014) and on wild animals to measure sexual dimorphism in Western gorillas (Breuer et al., 2007), shoulder heights of elephants (Schrader et al., 2006), nutritional status of Japanese macaques (Kurita et al., 2012), and the body condition of brown bears (Shirane et al., 2020). Over 70 years ago, Leedy (1948) encouraged wildlife biologists to use aerial photogrammetry from aircraft for censusing wild animal populations and their habitats, where photographs can be collected at nadir (straight down) or an oblique angle, and the scale can be calculated by dividing the focal length of the camera by the altitude or by using a ratio of selected points in an image of a known size. Indeed, aerial photogrammetry has been wildly adopted by wildlife biologists and has proven useful in obtaining measurements in large vertebrates, such as elephants and whales.

Whitehead & Payne (1978) first demonstrated the utility of using aerial photogrammetry from airplanes and helicopters as a non-invasive technique for estimating the body length of southern right whales. Prior to this technique, measurements of whales were traditionally limited to assessing carcasses collected from scientific whaling operations, or opportunistically from commercial whaling, subsistence hunting, stranding events, and bycatch. Importantly, aerial photogrammetry provides a method to collect measurements of whales without killing them. This approach has been widely adopted to obtain body length measurements on a variety of whale and dolphin species, including bowhead whales (Cubbage & Calambokidis, 1987), southern right whales (Best & Rüther, 1992), fin whales (Ratnaswamy and Wynn, 1993), common dolphins (Perryman and Lynn, 1993), spinner dolphins (Perryman & Westlake 1998), and killer whales (Fearnbach et al. 2012). Aerial photogrammetry has also been used to measure body widths to estimate nutritive condition related to reproduction in gray whales (Perryman and Lynn, 2002) and northern and southern right whales (Miller et al., 2012). However, these studies collected photographs from airplanes and helicopters, which can be costly, limited by weather and infrastructure to support aircraft research efforts and, importantly, presents a potential risk to wildlife biologists (Sasse 2003). 

The recent advancement and commercialization of unoccupied aircraft systems (UAS, or drones) has revolutionized the ability to obtain morphological measurements from high resolution aerial photogrammetry across a variety of ecosystems (Fig. 2). Drones ultimately bring five transformative qualities to conservation science compared to airplanes and helicopters: affordability, immediacy, quality, efficiency, and safety of data collection. Durban et al. (2015) first demonstrated the utility of using drones for non-invasively obtaining morphological measurements of killer whales in remote environments. Since then, drone-based morphological measurements have been applied to a wide range of studies that have increased our understanding on different whale populations. For example, Leslie et al. (2020) used drone-based measurements of the skull to distinguish a unique sub-species of blue whales off the coast of Chile. Groskreutz et al. (2019) demonstrated how long-term nutritional stress has limited body growth in northern resident killer whales, while Stewart et al. (2021) found a decrease in body length of North Atlantic Right whales since 1981 that was associated with entanglements from fishing gear and may be a contributing factor to the decrease in reproductive success for this endangered population. 

Drone imagery is commonly used to estimate the body condition of baleen whales by measuring the body length and width of individuals. Recently, the GEMM Lab used body length and width measurements to quantify intra- and inter-seasonal changes in body condition across individual gray whales (Lemos et al., 2020). Drones have also been used to measure body condition loss in humpback whales during the breeding season (Christiansen et al., 2016) and to compare the healthy southern right whales to the skinnier, endangered North Atlantic right whales (Christiansen et al., 2020). Drone-based assessments of body condition have even been used to measure how calf growth rate is directly related to maternal loss during suckling (Christiansen et al., 2018), and even estimate body mass (Christiansen et al., 2019). 

Drone-based morphological measurements can also be combined with whale-borne inertial sensing tag data to study the functional morphology across several different baleen whale species. Kahane-Rapport et al. (2020) used drone measurements of tagged whales to analyze the biomechanics of how larger whales require longer times for filtering the water through their baleen when feeding. Gough et al. (2019) used size measurements from drones and swimming speeds from tags to determine that a whale’s “walking speed” is 2 meters per second – whether the largest of the whales, a blue whale, or the smallest of the baleen whales, an Antarctic minke whale. Size measurements and tag data were combined by Segre et al. (2019) to quantify the energetic costs of different sized whales when breaching. 

Taken together, drones have revolutionized our ability to obtain morphological measurements of whales, greatly increasing our capacity to better understand how these animals function and perform in their environments. These advancements in marine science are particularly important as these methods provide greater opportunity to monitor the health of populations, especially as they face increased threats from anthropogenic stressors (such as vessel traffic, ocean noise, pollution, fishing entanglement, etc.) and climate change. 

Drone-based photogrammetry is one of the main focuses of the GEMM Lab’s project on Gray whale Response to Ambient Noise Informed by Technology and Ecology (GRANITE). This summer we have been collecting drone videos to measure the body condition of gray whales feeding off the coast of Newport, Oregon (Fig. 2). As we try to understand the physiological stress response of gray whales to noise and other potential stressors, we have to account for the impacts of overall nutritional state of each individual whale’s physiology, which we infer from these body condition estimates. 

Figure 2. Drones can help collect images of whales to obtain morphological measurements using photogrammetry and help us fill knowledge gaps for how these animals interact in their environment and to assess their current health. Bottom photo is an image collected by the GEMM Lab of a gray whale being measured in MorphoMetriX software to estimate its body condition. 

References

Best, P. B., & Rüther, H. (1992). Aerial photogrammetry of southern right whales, Eubalaena australis. Journal of Zoology228(4), 595-614.

Breuer, T., Robbins, M. M., & Boesch, C. (2007). Using photogrammetry and color scoring to assess sexual dimorphism in wild western gorillas (Gorilla gorilla). American Journal of Physical Anthropology134(3), 369–382. https://doi.org/10.1002/ajpa.20678 

Christiansen, F., Vivier, F., Charlton, C., Ward, R., Amerson, A., Burnell, S., & Bejder, L. (2018). Maternal body size and condition determine calf growth rates in southern right whales. Marine Ecology Progress Series592, 267–281. 

Christiansen, F. (2020). A population comparison of right whale body condition reveals poor state of North Atlantic right whale, 1–43. 

Christiansen, F., Dujon, A. M., Sprogis, K. R., Arnould, J. P. Y., & Bejder, L. (2016). Noninvasive unmanned aerial vehicle provides estimates of the energetic cost of reproduction in humpback whales. Ecosphere7(10), e01468–18. 

Christiansen, F., Sironi, M., Moore, M. J., Di Martino, M., Ricciardi, M., Warick, H. A., … Uhart, M. M. (2019). Estimating body mass of free-living whales using aerial photogrammetry and 3D volumetrics. Methods in Ecology and Evolution10(12), 2034–2044. 

Cubbage, J. C., & Calambokidis, J. (1987). Size-class segregation of bowhead whales discerned through aerial stereo-photogrammetry. Marine Mammal Science3(2), 179–185. 

De Meyer, J., Verhelst, P., & Adriaens, D. (2020). Saving the European Eel: How Morphological Research Can Help in Effective Conservation Management. Integrative and Comparative Biology23, 347–349. 

Gaudioso, V., Sanz-Ablanedo, E., Lomillos, J. M., Alonso, M. E., Javares-Morillo, L., & Rodr\’\iguez, P. (2014). “Photozoometer”: A new photogrammetric system for obtaining morphometric measurements of elusive animals, 1–10.

Gough, W. T., Segre, P. S., Bierlich, K. C., Cade, D. E., Potvin, J., Fish, F. E., … Goldbogen, J. A. (2019). Scaling of swimming performance in baleen whales. Journal of Experimental Biology222(20), jeb204172–11. 

Groskreutz, M. J., Durban, J. W., Fearnbach, H., Barrett-Lennard, L. G., Towers, J. R., & Ford, J. K. B. (2019). Decadal changes in adult size of salmon-eating killer whales in the eastern North Pacific. Endangered Species Research40, 1 

Kahane-Rapport, S. R., Savoca, M. S., Cade, D. E., Segre, P. S., Bierlich, K. C., Calambokidis, J., … Goldbogen, J. A. (2020). Lunge filter feeding biomechanics constrain rorqual foraging ecology across scale. Journal of Experimental Biology223(20), jeb224196–8. 

Leedy, D. L. (1948). Aerial Photographs, Their Interpretation and Suggested Uses in Wildlife Management. The Journal of Wildlife Management12(2), 191. 

Lemos, L. S., Burnett, J. D., Chandler, T. E., Sumich, J. L., and Torres, L. G. (2020). Intra- and inter-annual variation in gray whale body condition on a foraging ground. Ecosphere 11.

Leslie, M. S., Perkins-Taylor, C. M., Durban, J. W., Moore, M. J., Miller, C. A., Chanarat, P., … Apprill, A. (2020). Body size data collected non-invasively from drone images indicate a morphologically distinct Chilean blue whale (Balaenoptera musculus) taxon. Endangered Species Research43, 291–304. 

Miles, D. B. (2020). Can Morphology Predict the Conservation Status of Iguanian Lizards? Integrative and Comparative Biology

Miller, C. A., Best, P. B., Perryman, W. L., Baumgartner, M. F., & Moore, M. J. (2012). Body shape changes associated with reproductive status, nutritive condition and growth in right whales Eubalaena glacialis and E. australis. Marine Ecology Progress Series459, 135–156. 

Negretti, P., Bianconi, G., Bartocci, S., Terramoccia, S., & Verna, M. (2008). Determination of live weight and body condition score in lactating Mediterranean buffalo by Visual Image Analysis. Livestock Science113(1), 1–7. https://doi.org/10.1016/j.livsci.2007.05.018 

Ratnaswamy, M. J., & Winn, H. E. (1993). Photogrammetric Estimates of Allometry and Calf Production in Fin Whales, \emph{Balaenoptera physalus}. American Society of Mammalogists74, 323–330. 

Perryman, W. L., & Lynn, M. S. (1993). Idendification of geographic forms of common dolphin(\emph{Delphinus Delphis}) from aerial photogrammetry. Marine Mammal Science9(2), 119–137. 

Perryman, W. L., & Lynn, M. S. (2002). Evaluation of nutritive condition and reproductive status of migrating gray whales (\emph{Eschrichtius robustus}) based on analysisof photogrammetric data. Journal Cetacean Research and Management4(2), 155–164. 

Perryman, W. L., & Westlake, R. L. (1998). A new geographic form of the spinner dolphin, stenella longirostris, detected with aerial photogrammetry. Marine Mammal Science14(1), 38–50. 

Sasse, B. (2003). Job-Related Mortality of Wildlife Workers in the United States, 1937- 2000, 1015–1020. 

Segre, P. S., Potvin, J., Cade, D. E., Calambokidis, J., Di Clemente, J., Fish, F. E., … & Goldbogen, J. A. (2020). Energetic and physical limitations on the breaching performance of large whales. Elife9, e51760.

Shirane, Y., Mori, F., Yamanaka, M., Nakanishi, M., Ishinazaka, T., Mano, T., … Shimozuru, M. (2020). Development of a noninvasive photograph-based method for the evaluation of body condition in free-ranging brown bears. PeerJ8, e9982. https://doi.org/10.7717/peerj.9982 

Shrader, A. M., M, F. S., & Van Aarde, R. J. (2006). Digital photogrammetry and laser rangefinder techniques to measure African elephants, 1–7. 

Stewart, J. D., Durban, J. W., Knowlton, A. R., Lynn, M. S., Fearnbach, H., Barbaro, J., … & Moore, M. J. (2021). Decreasing body lengths in North Atlantic right whales. Current Biology.

Walker, J. A., Alfaro, M. E., Noble, M. M., & Fulton, C. J. (2013). Body fineness ratio as a predictor of maximum prolonged-swimming speed in coral reef fishes. PloS one8(10), e75422.

The learning curve never stops as the GRANITE project begins its seventh field season

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

When I thought about what doing fieldwork would be like, before having done it myself, I imagined that it would be a challenging, but rewarding and fun experience (which it is). However, I underestimated both ends of the spectrum. I simultaneously did not expect just how hard it would be and could not imagine the thrill of working so close to whales in a beautiful place. One part that I really did not consider was the pre-season phase. Before we actually get out on the boats, we spend months preparing for the work. This prep work involves buying gear, revising and developing protocols, hiring new people, equipment maintenance and testing, and training new skills. Regardless of how many successful seasons came before a project, there are always new tasks and challenges in the preparation phase.

For example, as the GEMM Lab GRANITE project team geared up for its seventh field season, we had a few new components to prepare for. Just to remind you, the GRANITE (Gray whale Response to Ambient Noise Informed by Technology and Ecology) project’s field season typically takes place from June to mid-October of each year. Throughout this time period the field team goes out on a small RHIB (rigid hull inflatable boat), whenever the weather is good enough, to collect photo-ID data, fecal samples, and drone imagery of the Pacific Coast Feeding Group (PCFG) gray whales foraging near Newport, OR, USA. We use the data to assess the health, ecology and population dynamics of these whales, with our ultimate goal being to understand the effect of ambient noise on the population. As previous blogs have described, a typical field day involves long hours on the water looking for whales and collecting data. This year, one of our exciting new updates is that we are going out on two boats for the first part of the field season and starting our season 10 days early (our first day was May 20th). These updates are happening because a National Science Foundation funded seismic survey is being conducted within our study area starting in June. The aim of this survey is to assess geophysical structures but provides us with an opportunity to assess the effect of seismic noise on our study group by collecting data before, during, and after the survey. So, we started our season early in order to capture the “before seismic survey” data and we are using a two-boat approach to maximize our data collection ability.

While this is a cool opportunistic project, implementing the two-boat approach came with a new set of challenges. We had to find a second boat to use, buy a new set of gear for the second boat, figure out the best way to set up our gear on a boat we had not used before, and update our data processing protocols to include data collected from two boats on the same day. Using two boats also means that everyone on the core field team works every day. This core team includes Leigh (lab director/fearless leader), Todd (research assistant), Lisa (PhD student), Ale (new post-doc), and me (Clara, PhD student). Leigh and Todd are our experts in boat driving and working with whales, Todd is our experienced drone pilot, I am our newly certified drone pilot, and Lisa, Ale, and myself are boat drivers. Something I am particularly excited about this season is that Lisa, Ale, and I all have at least one field season under our belts, which means that we get to become more involved in the process. We are learning how to trailer and drive the boats, fly the drones, and handling more of the post-field work data processing. We are becoming more involved in every step of a field day from start to finish, and while it means taking on more responsibility, it feels really exciting. Throughout most of graduate school, we grow as researchers as we develop our analytical and writing skills. But it’s just as valuable to build our skillset for field work. The ocean conditions were not ideal on the first day of the field season, so we spent our first day practicing our field skills.

For our “dry run” of a field day, we went through the process of a typical day, which mostly involved a lot of learning from Leigh and Todd. Lisa practiced her trailering and launching of the boat (figure 1), Ale and Lisa practiced driving the boat, and I practiced flying the drone (figure 2). Even though we never left the bay or saw any whales, I thoroughly enjoyed our dry run. It was useful to run through our routine, without rushing, to get all the kinks out, and it also felt wonderful to be learning in a supportive environment. Practicing new skills is stressful to say the least, especially when there is expensive equipment involved, and no one wants to mess up when they’re being watched. But our group was full of support and appreciation for the challenges of learning. We cheered for successful boat launchings and dockings, and drone landings. I left that day feeling good about practicing and improving my drone piloting skills, full of gratitude for our team and excited for the season ahead.

Figure 1. Lisa (driving the truck) launching the boat.
Figure 2. Clara (seated, wearing a black jacket) landing the drone in Ale’s hands.

All the diligent prep work paid off on Saturday with a great first day (figure 3). We conducted five GoPro drops (figure 4), collected seven fecal samples from four different whales (figure 5), and flew four drone flights over three individuals including our star from last season, Sole. Combined, we collected two trifectas (photo-ID images, fecal samples, and drone footage)! Our goal is to get as many trifectas as possible because we use them to study the relationship between the drone data (body condition and behavior) and the fecal sample data (hormones). We were all exhausted after 10 hours on the water, but we were all very excited to kick-start our field season with a great day.

Figure 3. Lisa on the bow pulpit during our first sighting of the day.
Figure 4. Lisa doing a GoPro drop, she’s lowering the GoPro into the water using the line in her hands.
Figure 5. Clara and Ale collecting a fecal sample.

On Sunday, just one boat went out to collect more data from Sole after a rainy morning and I successfully flew over her from launching to landing! We have a long season ahead, but I am excited to learn and see what data we collect. Stay tuned for more updates from team GRANITE as our season progresses!

Milling around in definitions

Clara Bird, Masters Student, OSU Department of Fisheries and Wildlife, Geospatial Ecology of Marine Megafauna Lab

A big part of graduate school involves extensive reading to learn about the previous research conducted in the field you are joining and the embedded foundational theories. A firm understanding of this background literature is needed in order to establish where your research fits. Science is a constructive process; to advance our disciplines we must recognize and build upon previous work. Hence, I’ve been reading up on the central topic of my thesis: behavioral ecology. It is equally important to study the methods used in these studies as to understand the findings. As discussed in a previous blog, ethograms are a central component of the methodology for studying behavior. Ethograms are lists of defined behaviors that help us properly and consistently collect data in a standardized approach. It is especially important in a project that spans years to know that the data collected at the beginning was collected in the same way as the data collected at the end of the project.

While ethograms and standardized methods are commonly used within a study, I’ve noticed from reading through studies on cetaceans, a lack of standardization across studies. Not all behaviors that are named the same way have matching definitions, and not all behaviors with similar definitions have matching names. Of all the behaviors, “milling” may be the least standardized.

While milling is not in our ethogram (Leigh believes this term is a “cheat” for when behavior is actually “unknown”), we occasionally use “milling” in the field to describe when the gray whales are swimming around in an area, not foraging, but not in any other primary behavior state (travel, social, or rest). Sometimes we use when we think the whale may be searching, but we aren’t 100% sure yet. A recent conversation during a lab meeting on the confusing nature of the term “milling” inspired me to dig into the literature for this blog. I searched through the papers I’ve saved for my literature review and found 18 papers that used the term milling. It was fascinating to read how variably the term has been defined and used.

When milling was defined in these papers, it was most commonly described as numerous directional changes in movement within a restricted area 1–8. Milling often co-occurred with other behavior states. Five of these eight studies described milling as co-occurring with foraging behavior 3–6,8. In one case, milling was associated with foraging and slow movement 8. While another study described milling as passive, slow, nondirectional movement 9.

Eight studies used the term milling without defining the behavior 10–17. Of these, five described milling as being associated with other behavior states. Three studies described milling as co-occurring with foraging 10,14,16, one said that it co-occurred with social behavior 13, and another described milling as being associated with resting/slow movement 12.

In addition to this variety of definitions and behavior associations, there were also inconsistencies with the placement of “milling” within ethograms. In nine studies, milling was listed as a primary state 1,2,4,7–9,15,17,18. But, in two studies that mentioned milling and used an ethogram, milling was not included in the ethogram 6,14.

Diving into the associations between milling and foraging reveal how varied the use of milling has been within the cetacean literature. For example, two studies simply described milling as occurring near foraging in time 10,16. While another two studies explained that milling was applied in situations where there was evidence of feeding without feeding being directly observed 8,14. Bobkov et al. (2019) described milling as occurring between feeding cycles along with breathing. Lastly, two studies describe milling as a behavior within the foraging primary state 3,5, while another study described feeding as a behavior within milling 4.

It’s all rather confusing, huh? Across these studies, milling has been defined, mentioned without being defined, included in ethograms as a primary state, included in ethograms as a sub-behavior, and excluded from ethograms. Milling has also been associated with multiple primary behavior states (foraging, resting, and socializing). It has been described as both passive 9 and slow 12, and strong 16 and active 5.

It appears that milling is often used to describe behaviors that the observer cannot distinctly classify or describe its function. I have also struggled to define these times when a whale is in between behavior states; I often end up calling it “just being a whale”, which includes time spent breathing at the surface, or just swimming around.

As I’ve said above, Leigh thinks that this term is a “cheat” for when a behavior is actually “unknown”. I think we have trouble equating “milling” with “unknown” because it seems like “unknown” should refer to a behavior where we can’t quite tell what the whale is doing. However, during milling, we can see that the whale is swimming at the surface. But here’s the thing, while we can see what the whale is doing, the function of the behavior is still unknown. Instead of using an indistinct term, we should use a term that better describes the behavior.  If it’s swimming at the surface, name the behavior “swimming at the surface”. If we can’t tell what the whale is doing because we can’t quite see what it’s doing, then name the behavior “unknown-partially visible”. Instead of using vague terminology, we should use clear names for behaviors and embrace using the term “unknown”.

I am most certainly not criticizing these studies as they all provided valuable contributions and interesting results. The studies that asked questions about behavioral ecology defined milling. The term was mentioned without being defined in studies focused on other topics. So, defining behaviors mentioned was less important.

With this exploration into the use of “milling” in studies, I am not implying that all behavioral ecologists need to agree on the use of the same behavior terms. However, I have learned clear definitions are critical. This lesson is also important outside of behavioral ecology. Different labs, and different people, use different terms for the same things. As I dig into my thesis, I am keeping a list of terminology I use and how I define those terms, because as I learn more, my terminology evolves and changes. For example, at the beginning of my thesis I used “sub-behavior” to refer to behaviors within the primary state categories. But, now after chatting with Leigh and learning more, I’ve decided to use the term “tactic” instead as these are often processes or events that contribute to the broader behavior state. My running list of terminology helps me remember what I meant when I used a certain word, so that when I read my notes from three months ago, I can know what I meant.  Digging into the literature for this blog reminded me of the importance of clearly defining all terminology and never assuming that everyone uses the same term in the same way.

Check out these videos to see some of the behaviors we observe:

References

1.        Mallonee, J. S. Behaviour of gray whales (Eschrichtius robustus) summering off the northern California coast, from Patrick’s Point to Crescent City. Can. J. Zool. 69, 681–690 (1991).

2.        Clarke, J. T., Moore, S. E. & Ljungblad, D. K. Observations on gray whale (Eschrichtius robustus) utilization patterns in the northeastern Chukchi Sea. Can. J. Zool 67, (1988).

3.        Ingram, S. N., Walshe, L., Johnston, D. & Rogan, E. Habitat partitioning and the influence of benthic topography and oceanography on the distribution of fin and minke whales in the Bay of Fundy, Canada. J. Mar. Biol. Assoc. United Kingdom 87, 149–156 (2007).

4.        Lomac-MacNair, K. & Smultea, M. A. Blue Whale (Balaenoptera musculus) Behavior and Group Dynamics as Observed from an Aircraft off Southern California. Anim. Behav. Cogn. 3, 1–21 (2016).

5.        Lusseau, D., Bain, D. E., Williams, R. & Smith, J. C. Vessel traffic disrupts the foraging behavior of southern resident killer whales Orcinus orca. Endanger. Species Res. 6, 211–221 (2009).

6.        Bobkov, A. V., Vladimirov, V. A. & Vertyankin, V. V. Some features of the bottom activity of gray whales (Eschrichtius robustus) off the northeastern coast of Sakhalin Island. 1, 46–58 (2019).

7.        Howe, M. et al. Beluga, Delphinapterus leucas, ethogram: A tool for cook inlet beluga conservation? Mar. Fish. Rev. 77, 32–40 (2015).

8.        Clarke, J. T., Christman, C. L., Brower, A. A. & Ferguson, M. C. Distribution and Relative Abundance of Marine Mammals in the northeastern Chukchi and western Beaufort Seas, 2012. Annu. Report, OCS Study BOEM 117, 96349–98115 (2013).

9.        Barendse, J. & Best, P. B. Shore-based observations of seasonality, movements, and group behavior of southern right whales in a nonnursery area on the South African west coast. Mar. Mammal Sci. 30, 1358–1382 (2014).

10.      Le Boeuf, B. J., M., H. P.-C., R., J. U. & U., B. R. M. and F. O. High gray whale mortality and low recruitment in 1999: Potential causes and implications. (Eschrichtius robustus). J. Cetacean Res. Manag. 2, 85–99 (2000).

11.      Calambokidis, J. et al. Abundance, range and movements of a feeding aggregation of gray whales (Eschrictius robustus) from California to southeastern Alaska in 1998. J. Cetacean Res. Manag. 4, 267–276 (2002).

12.      Harvey, J. T. & Mate, B. R. Dive Characteristics and Movements of Radio-Tagged Gray Whales in San Ignacio Lagoon, Baja California Sur, Mexico. in The Gray Whale: Eschrichtius Robustus (eds. Jones, M. Lou, Folkens, P. A., Leatherwood, S. & Swartz, S. L.) 561–575 (Academic Press, 1984).

13.      Lagerquist, B. A. et al. Feeding home ranges of pacific coast feeding group gray whales. J. Wildl. Manage. 83, 925–937 (2019).

14.      Barrett-Lennard, L. G., Matkin, C. O., Durban, J. W., Saulitis, E. L. & Ellifrit, D. Predation on gray whales and prolonged feeding on submerged carcasses by transient killer whales at Unimak Island, Alaska. Mar. Ecol. Prog. Ser. 421, 229–241 (2011).

15.      Luksenburg, J. A. Prevalence of External Injuries in Small Cetaceans in Aruban Waters, Southern Caribbean. PLoS One 9, e88988 (2014).

16.      Findlay, K. P. et al. Humpback whale “super-groups” – A novel low-latitude feeding behaviour of Southern Hemisphere humpback whales (Megaptera novaeangliae) in the Benguela Upwelling System. PLoS One 12, e0172002 (2017).

17.      Villegas-Amtmann, S., Schwarz, L. K., Gailey, G., Sychenko, O. & Costa, D. P. East or west: The energetic cost of being a gray whale and the consequence of losing energy to disturbance. Endanger. Species Res. 34, 167–183 (2017).

18.      Brower, A. A., Ferguson, M. C., Schonberg, S. V., Jewett, S. C. & Clarke, J. T. Gray whale distribution relative to benthic invertebrate biomass and abundance: Northeastern Chukchi Sea 2009–2012. Deep. Res. Part II Top. Stud. Oceanogr. 144, 156–174 (2017).

How we plan to follow whales

Clara Bird, Masters Student, OSU Department of Fisheries and Wildlife, Geospatial Ecology of Marine Megafauna Lab

The GEMM Lab gray whale team is in the midst of preparing for our fifth field season studying the Pacific Coast Foraging Group (PCFG): whales that forage off the coast of Newport, OR, USA each summer. On any given good weather day from June to October, our team is out on the water in a small zodiac looking for gray whales (Figure 1). When we find a gray whale, we try to collect photo ID data, fecal samples, drone data, and behavioral data. We use the drone data to study both the whale’s body condition and their behavior. In a previous blog, I described ethograms and how I would like to use the behavior data from drone videos to classify behaviors, with the ultimate goal of understanding how gray whale behavior varies across space, time, and by individual. However, this explanation of studying whale behavior is actually a bit incomplete. Before we start fieldwork, we first need to decide how to collect that data.

Figure 1. Image of GEMM lab team collecting gray whale UAS data. Image taken under NOAA/NMFS permit #16111

As observers, we are far from omnipresent and there is no way to know what the animals are doing all of the time. In any environment, scientists have to decide when and where to observe their animals and what behaviors they are interested in recording. In many studies, behavior is recorded live by an observer. In those studies, other limitations need to be taken into account, such as human error and observer fatigue. Collecting behavioral data is particularly challenging in the marine environment. Cetaceans spend most of their lives out of sight from humans, their time at the surface is brief, and when they appear together in large groups it can be very difficult to keep track of who is doing what when. Imagine being in a boat trying to keep track of what three different whales are doing without a pre-determined method – the task could quickly become overwhelming and biased. This is why we need a methodology for collecting and classifying behavior. We cannot study behavior without acknowledging these limitations and the potential biases that come with the methods we choose. Different data collection methods are better suited to address different questions.

The use of drones gives us the ability to record cetacean behavior non-invasively, from a perspective that allows greater observation (Figure 2, Torres et al. 2018), and for later review, which is a significant improvement. However, as we prepare to collect more behavior data, we need to study the methods and understand the benefits and disadvantages of each approach so that we capture the information we need without bias. Altmann (1974) provides a thorough overview of behavioral sampling methods.

Figure 2. Diagram illustrating “whale surface time” relative to “whale visible time” data as collected from an unmanned aerial systems (UAS) aircraft flying over a gray whale as it moves sequentially (from right to left) from “headstand” foraging to surfacing. Figure from Torres et al. (2018).

Ad libitum behavioral sampling has no structure and occurs when we find a group of whales and just write down everything they are doing. This method is a good first step, however it comes with bias.  Without structure, we cannot be sure that there was an equal probability of detecting each kind of behavior; this problem is called detectability bias. This type of bias is an issue if we are trying to answer questions about how often a behavior occurs, or what percent of time is spent in each behavior state. This is a bias to be especially concerned about when it comes to cetaceans because there are many examples of behaviors with different levels of detectability. An extreme example would be the detectability of breaching versus a behavior that takes place under the surface. A breaching whale is easier to spot and more exciting, which could lead to results suggesting that whales breach more often than they do relative to underwater behaviors. While it’s impossible to eliminate detectability bias, other sampling methods employ decision rules to try and reduce its effect. Many decision rules revolve around time, such as setting a minimum or maximum observation time interval. Other time rules involve recording the behavior state at set intervals of time (e.g., every 5 minutes). Setting observation boundaries helps standardize the methods and the data being collected.

In a structured sampling plan, the first big decision that needs to be addressed is the need to know the duration of behaviors. Point events do not include duration data but can be used to study the frequencies of behaviors. For example, if my research question was “Do whales perform “headstands” in a specific habitat type?”, then I would need point events of headstanding behavior. But, if I wanted to ask, “Do whales spend more time spent headstanding in a specific habitat type than in other habitat types?”, I would need headstanding to be a state event. State events are events with associated duration information and can be used for activity budgets. Activity budgets show how much time an animal spends in each behavior state. Some sampling methods focus on collecting only point events. However, to get the most complete understanding of behavior I think it’s important to collect both. Focal animal follows are another method of collecting more detailed data and is commonly used in cetacean studies.

The explanation of a focal follow method is in the name.  We focus on one individual, follow it, and record all of its behaviors. When employing this method, decisions are made about how an individual is chosen and how long it is followed. In some cases, the behavior of this animal is used as a proxy for the behavior of an entire group. I essentially use the focal follow method in my research. While I review drone footage to record behavioral data instead of recording behaviors live in the field, I focus on one individual a time as I go through the videos. To do this I use a software called BORIS (Friard and Gamba 2016) to mark the time of each behavior per individual (Figure 3). If there are three individuals in a video, I’ll review the footage three times to record behaviors once per individual, focusing on each in turn.

Figure 3. Screenshot of BORIS layout.

While the drone footage brings the advantages of time to review and a better view of the whale, we are constrained by the duration of a flight. Focal follows would ideally last longer than the ~15 minutes of battery life per drone flight. Our previously collected footage gives us snapshots of behavior, and this makes it challenging to compare and analyze durations of behaviors. Therefore, I am excited that we are going to try conducting drone focal follows this summer by swapping out drones when power runs low to achieve longer periods of video coverage of whale behavior. I’ll be able to use these data to move from snapshots to analyzing longer clips and better understanding the behavioral ecology of gray whales. As exciting as this opportunity is, it also presents the challenge of method development. So, I now need to develop decision rules and data collection methods to answer the questions that I have been eagerly asking.

References

Altmann, Jeanne. 1974. “Observational Study of Behavior: Sampling Methods.” Behaviour 49 (3–4): 227–66. https://doi.org/10.1163/156853974X00534.

Friard, Olivier, and Marco Gamba. 2016. “BORIS: A Free, Versatile Open-Source Event-Logging Software for Video/Audio Coding and Live Observations.” Methods in Ecology and Evolution 7 (11): 1325–30. https://doi.org/10.1111/2041-210X.12584.

Torres, Leigh G., Sharon L. Nieukirk, Leila Lemos, and Todd E. Chandler. 2018. “Drone up! Quantifying Whale Behavior from a New Perspective Improves Observational Capacity.” Frontiers in Marine Science 5 (SEP). https://doi.org/10.3389/fmars.2018.00319.

Snacks at the surface: New GEMM Lab publication reveals insights into blue whale surface foraging through drone observations and prey data

By Dawn Barlow, PhD student, OSU Department of Fisheries and Wildlife, Geospatial Ecology of Marine Megafauna Lab

As the largest animals on the planet, blue whales have massive prey requirements to meet energy demands. Despite their enormity, blue whales feed on a tiny but energy-rich prey source: krill. Furthermore, they are air-breathing mammals searching for aggregations of prey in the expansive and deep ocean, and must therefore budget breath-holding and oxygen consumption, the travel time it takes to reach prey patches at depth, the physiological constraints of diving, and the necessary recuperation time at the surface. Additionally, blue whales employ an energetically demanding foraging strategy known as lunge feeding, which is only efficient if they can locate and target dense prey aggregations that compensate for the energetic costs of diving and lunging. In our recent paper, published today in PeerJ, we examine how blue whales in New Zealand optimize their energy use through preferentially feeding on dense krill aggregations near the water’s surface.

Figure 1. A blue whale lunges on a dense aggregation of krill at the surface. Note the krill jumping away from the mouth of the onrushing whale. UAS piloted by Todd Chandler.
Figure 2. Survey tracklines in 2017 in the South Taranaki Bight (STB) with locations of blue whale sightings, and where surface lunge feeding was observed, denoted. Inset map shows location of the STB within New Zealand. Figure reprinted from Torres et al. 2020.

To understand how predators such as blue whales optimize foraging strategies, knowledge of predator behavior and prey distribution is needed. In 2017, we surveyed for blue whales in New Zealand’s South Taranaki Bight region (STB, Fig. 2) while simultaneously collecting prey distribution data using an echosounder, which allowed us to identify the location, depth, and density of krill aggregations throughout the region. When blue whales were located, we observed their behavior from the research vessel, recorded their dive times, and used an unmanned aerial system (UAS; “drone”) to assess their body condition and behavior.

Much of what is known about blue whale foraging behavior and energetics comes from extensive studies off the coast of California, USA using accelerometer tags to track fine-scale kinematics (i.e., body movements) of the whales. In the California Current, the krill species targeted by blue whales are denser at depth, and therefore blue whales regularly dive to depths of 300 meters to lunge on the most energy-rich prey aggregations. However, given the reduced energetic costs of feeding closer to the surface, optimal foraging theory predicts that blue whales should only forage at depth when the energetic gain outweighs the cost. In New Zealand, we found that blue whales foraged where krill aggregations were relatively shallow and dense compared to the availability of krill across the whole study area (Fig. 3). Their dive times were quite short (~2.5 minutes, compared to ~10 minutes in California), and became even shorter in locations where foraging behavior and surface lunge feeding were observed.

Figure 3. Density contours comparing the depth and density (Sv) of krill aggregations at blue whale foraging sightings (red shading) and in absence of blue whales (gray shading). Density contours: 25% = darkest shade, 755 = medium shade, 95% = light shade. Blue circles indicate krill aggregations detected within 2 km of the sighting of the UAS filmed surface foraging whale analyzed in this study. Figure reprinted from Torres et al. 2020.
Figure 4. Kinematics of a blue whale foraging dive derived from a suction cup tag. Upper panel shows the dive profile (yellow line), with lunges highlighted (green circles), superimposed on a prey field map showing qualitative changes in krill density (white, low; blue, medium; red, high). The lower panels show the detailed kinematics during lunges at depth. Here, the dive profile is shown by a black line. The orange line shows fluking strokes derived from the accelerometer data, the green line represents speed estimated from flow noise, and the grey circles indicate the speed calculated from the vertical velocity of the body divided by the sine of the body pitch angle, which is shown by the red line. Figure and caption reprinted from Goldbogen et al. 2011.

Describing whale foraging behavior and prey in the surface waters has been difficult due to logistical limitations of conventional data collection methods, such as challenges inferring surface behavior from tag data and quantifying echosounder backscatter data in surface waters. To compliment these existing methods and fill the knowledge gap surrounding surface behavior, we highlight the utility of a different technological tool: UAS. By analyzing video footage of a surface lunge feeding sequence, we obtained estimates of the whale’s speed, acceleration, roll angle, and head inclination, producing a figure comparable to what is typically obtained from accelerometer tag data (Fig. 4, Fig. 5). Furthermore, the aerial perspective provided by the UAS provides an unprecedented look at predator-prey interactions between blue whales and krill. As the whale approaches the krill patch, she first observes the patch with her right eye, then turns and lines up her attack angle to engulf almost the entire prey patch through her lunge. Furthermore, we can pinpoint the moment when the krill recognize the impending danger of the oncoming predator—at a distance of 2 meters, and 0.8 seconds before the whale strikes the patch, the krill show a flee response where they leap away from the whale’s mouth (see video, below).

Figure 5. Body kinematics during blue whale surface lunge feeding event derived from Unmanned Aerial Systems (UAS) image analysis. (A) Mean head inclination and roll (with CV in shaded areas), (B) relative speed and acceleration, and (C) distance from the tip of the whale’s rostrum to the nearest edge of krill patch. Blue line on plots indicate when krill first respond to the predation event, and the purple dashed lines indicate strike at time = 0. The orange lines indicate the time at which the whale’s gape is widest, head inclination is maximum, and deceleration is greatest. Figure reprinted from Torres et al. 2020

In this study, we demonstrate that surface waters provide important foraging opportunities and play a key role in the ecology of New Zealand blue whales. The use of UAS technology could be a valuable and complimentary tool to other technological approaches, such as tagging, to gain a comprehensive understanding of foraging behavior in whales.

To see the spectacle of a blue whale surface lunge feeding, we invite you to take a look at the video footage, below:

The publication is led by GEMM Lab Principal Investigator Dr. Leigh Torres. I led the prey data analysis portion of the study, and co-authors include our drone pilot extraordinaire Todd Chandler and UAS analysis guru Dr. Jonathan Burnett. We are grateful to all who assisted with fieldwork and data collection, including Kristin Hodge, Callum Lilley, Mike Ogle, and the crew of the R/V Star Keys (Western Workboats, Ltd.). Funding for this research was provided by The Aotearoa Foundation, The New Zealand Department of Conservation, The Marine Mammal Institute at Oregon State University, Greenpeace New Zealand, OceanCare, Kiwis Against Seabed Mining, The International Fund for Animal Welfare, and The Thorpe Foundation.

Read Oregon State University’s press release about the publication here.

The complex relationship between behavior and body condition

Clara Bird, Masters Student, OSU Department of Fisheries and Wildlife, Geospatial Ecology of Marine Megafauna Lab

Imagine that you are a wild foraging animal: In order to forage enough food to survive and be healthy you need to be healthy enough to move around to find and eat your food. Do you see the paradox? You need to be in good condition to forage, and you need to forage to be in good condition. This complex relationship between body condition and behavior is a central aspect of my thesis.

One of the great benefits of having drone data is that we can simultaneously collect data on the body condition of the whale and on its behavior. The GEMM lab has been measuring and monitoring the body condition of gray whales for several years (check out Leila’s blog on photogrammetry for a refresher on her research). However, there is not much research linking the body condition of whales to their behavior. Hence, I have expanded my background research beyond the marine world to looked for papers that tried to understand this connection between the two factors in non-cetaceans. The literature shows that there are examples of both, so let’s go through some case studies.

Ransom et al. (2010) studied the effect of a specific type of contraception on the behavior of a population of feral horses using a mixed model. Aside from looking at the effect of the treatment (a type of contraception), they also considered the effect of body condition. There was no difference in body condition between the treatment and control groups, however, they found that body condition was a strong predictor of feeding, resting, maintenance, and social behaviors. Females with better body condition spent less time foraging than females with poorer body condition. While it was not the main question of the study, these results provide a great example of taking into account the relationship between body condition and behavior when researching any disturbance effect.

While Ransom et al. (2010) did not find that body condition affected response to treatment, Beale and Monaghan (2004) found that body condition affected the response of seabirds to human disturbance. They altered the body condition of birds at different sites by providing extra food for several days leading up to a standardized disturbance. Then the authors recorded a set of response variables to a disturbance event, such as flush distance (the distance from the disturbance when the birds leave their location). Interestingly, they found that birds with better body condition responded earlier to the disturbance (i.e., when the disturbance was farther away) than birds with poorer body condition (Figure 1). The authors suggest that this was because individuals with better body condition could afford to respond sooner to a disturbance, while individuals with poorer body condition could not afford to stop foraging and move away, and therefore did not show a behavioral response. I emphasize behavioral response because it would have been interesting to monitor the vital rates of the birds during the experiment; maybe the birds’ heart rates increased even though they did not move away. This finding is important when evaluating disturbance effects and management approaches because it demonstrates the importance of considering body condition when evaluating impacts: animals that are in the worst condition, and therefore the individuals that are most vulnerable, may appear to be undisturbed when in reality they tolerate the disturbance because they cannot afford the energy or time to move away.

Figure 1.  Figure showing flush distance of birds that were fed (good body condition) and unfed (poor body condition).

These two studies are examples of body condition affecting behavior. However, a study on the effect of habitat deterioration on lizards showed that behavior can also affect body condition. To study this effect, Amo et al. (2007) compared the behavior and body condition of lizards in ski slopes to those in natural areas. They found that habitat deterioration led to an increased perceived risk of predation, which led to an increase in movement speed when crossing these deteriorated, “risky”, areas. In turn, this elevated movement cost led to a decrease in body condition (Figure 2). Hence, the lizard’s behavior affected their body condition.


Figure 2. Figure showing the difference in body condition of lizards in natural and deteriorated habitats.

Together, these case studies provide an interesting overview of the potential answers to the question: does body condition affect behavior or does behavior affect body condition? The answer is that the relationship can go both ways. Ransom et al. (2004) showed that regardless of the treatment, behavior of female horses differed between body conditions, indicating that regardless of a disturbance, body condition affects behavior. Beale and Monaghan (2004) demonstrated that seabird reactions to disturbance differed between body conditions, indicating that disturbance studies should take body condition into account. And, Amo et al. (2007) showed that disturbance affects behavior, which consequently affects body condition.

Looking at the results from these three studies, I can envision finding similar results in my gray whale research. I hypothesize that gray whale behavior varies by body condition in everyday circumstances and when the whale is disturbed. Yet, I also hypothesize that being disturbed will affect gray whale behavior and subsequently their body condition. Therefore, what I anticipate based on these studies is a circular relationship between behavior and body condition of gray whales: if an increase in perceived risk affects behavior and then body condition, maybe those affected individuals with poor body condition will respond differently to the disturbance. It is yet to be determined if a sequence like this could ever be detected, but I think that it is important to investigate.

Reading through these studies, I am ready and eager to start digging into these hypotheses with our data. I am especially excited that I will be able to perform this investigation on an individual level because we have identified the whales in each drone video. I am confident that this work will lead to some interesting and important results connecting behavior and health, thus opening avenues for further investigations to improve conservation studies.

References

Beale, Colin M, and Pat Monaghan. 2004. “Behavioural Responses to Human Disturbance: A Matter of Choice?” Animal Behaviour 68 (5): 1065–69. https://doi.org/10.1016/j.anbehav.2004.07.002.

Ransom, Jason I, Brian S Cade, and N. Thompson Hobbs. 2010. “Influences of Immunocontraception on Time Budgets, Social Behavior, and Body Condition in Feral Horses.” Applied Animal Behaviour Science 124 (1–2): 51–60. https://doi.org/10.1016/j.applanim.2010.01.015.

Amo, Luisa, Pilar López, and José Martín. 2007. “Habitat Deterioration Affects Body Condition of Lizards: A Behavioral Approach with Iberolacerta Cyreni Lizards Inhabiting Ski Resorts.” Biological Conservation 135 (1): 77–85. https://doi.org/10.1016/j.biocon.2006.09.020.

Our GEM(M), Ruby, is back in action!

By Lisa Hildebrand, MSc student, OSU Department of Fisheries and Wildlife, Geospatial Ecology of Marine Megafauna Lab

Every season, or significant period of time, usually has a distinct event that marks its beginning. For example, even though winter officially begins when the winter solstice occurs sometime between December 20 and December 23, many people often associate the first snowfall as the real start of winter. To mark the beginning of schooling, when children start 1stgrade in Germany (which is where I’m from), they receive something called a “Zuckertüte”, which translated means “sugar bag”. It is a large (sometimes as large as the child) cone-shaped container made of cardboard filled with toys, chocolates, sweets, school supplies and various other treats topped with a large bow.

Receiving my Zuckertüte in August of 2001 before starting 1st grade. Source: Ines Hildebrand.

I still remember (and even have) mine – it was almost as tall as I was, had a large Barbie printed on it (and a real one sitting on top of it) and was bright pink. And of course, while at a movie theatre, once the lights dim completely and the curtain surrounding the screen opens just a little further, members of the audience stop chit-chatting or sending text messages, everyone quietens down and puts their devices away – the film is about to start. There are hundreds upon thousands of examples like these – moments, events, days that mark the start of something.

In the past, the beginning of summer has always been tied to two things for me: the end of school and the chance to be outside in the sun for many hours and days. This reality has changed slightly since moving to Oregon. While I don’t technically have any classes during the summer, the work definitely won’t stop. There are still dozens of papers to read, samples to run in the lab, and data points to plot. For anyone from Oregon or the Pacific Northwest (PNW), it’s pretty well known that the weather can be a little unpredictable and variable, meaning that summer might not always be filled with sunny days. Despite somewhat losing these two “summer markers”, I have found a new event to mark the beginning of summer – the arrival of the gray whales.

Their propensity for coastal waters and near-shore feeding is part of what makes gray whales so unique and arguably “easier” to study than some other baleen whale species. Image captured under NOAA/NMFS permit #21678. Source: Leigh Torres.

 

It’s official – the gray whale field season is upon us! As many of you may already know, the GEMM Lab has two active gray whale research projects: investigating the impacts of ocean noise on gray whale physiology and exploring potential individual foraging specialization among the Pacific Coast Feeding Group (PCFG) gray whales. Both projects involve field work, with the former operating out of Newport and the latter taking place in Port Orford, both collecting photographs and a variety of samples and tracklines to study the PCFG, which is a sub-group of the larger Eastern North Pacific (ENP) population. June 1st is the widely accepted “cut-off date” for the PCFG whales, whereby gray whales seen after June 1st along the PNW coastline (specifically northern California, Oregon, Washington and British Columbia) are considered members of the PCFG. While this date is not the only qualifying factor for an individual to be considered a PCFG member, it is a good general rule of thumb. Since last week happened to be the first week of June, PI Leigh Torres, field technician Todd Chandler and myself launched out onto the Pacific Ocean in our trusty RHIB Ruby twice looking for gray whales, and it sure was a successful start to the season!

Even though I have done small boat-based field work before, every project and field team operates a little differently, which is why I was a little nervous at first. There are a lot of components to the Newport-based project as Leigh & co. assess gray whale physiology by collecting fecal samples, drone imagery and taking photographs, observing behavior patterns, as well as assessing local prey through GoPro footage and light traps. I wasn’t worried about the prey components of the research, since there is plenty of prey sampling involved in my Port Orford research, however I was worried about the whale side of things. I wasn’t sure whether I would be able to catch the drone as it returned back home to Ruby, fearing I might fumble and let it slip through my fingers. I also experienced slight déjà vu when handling the net we use to collect the fecal samples as I was forced to think back to some previous field work that involved collecting a biopsy dart with a net as well. During that project, I had somehow managed to get the end of the net stuck in the back of the boat and as I tried to scoop up the biopsy dart with the net-end, the pole became more and more stuck while the water kept dragging the net-end down and eventually the pole ended up snapping in my hands. On top of all this anxiety and work, trying to find your footing in a small RHIB like Ruby packed with lots of gear and a good amount of swell doesn’t make any of those tasks any easier.

However, as it turned out, none of my fears came to fruition. As soon as Todd fired up Ruby’s engine and we whizzed out and under the Newport bridge, I felt exhilarated. I love field work and was so excited to be out on the water again. During the two days I was able to observe multiple individuals of a species of whale that I find unique and fascinating.

Markings and pigmentation on the flukes are also unique to individuals and allow us to perform photo identification to track individuals over months and years. Image captured under NOAA/NMFS permit #21678. Source: Leigh Torres.

I felt back in my natural element and working with Leigh and Todd was rewarding and fun, as I have so much to learn from their years of experience and natural talent in the field dealing with stressful situations and juggling multiple components and gear. Even though I wasn’t out there collecting data for my own project, some of my observations did get me thinking about what I hope to focus on in my thesis – individualization. It is always interesting to see how differently whales will behave, whether due to the substrate we find them over, the water depths we find them in, or what their surfacing patterns are like. Although I still have six weeks to go until my field season starts and feel lucky to have the opportunity to help Leigh and Todd with the Newport field work, I am already looking forward to getting down to Port Orford in mid-July and starting the fifth consecutive gray whale field season down there.

But back to Newport – over the course of two days, we were able to deploy and retrieve one light trap to collect zooplankton, collect two fecal samples, perform two GoPro drops, fly the drone three times, and take hundreds of photos of whales. Leigh and Todd were both glad to be reunited with an old friend while I felt lucky to be able to meet such a famous lady – Scarback. A whale with a long sighting history not just for the GEMM Lab but for various researchers along the coast that study this population. Scarback is well-known (and easily identified) by the large concave injury on her back that is covered in whale lice, or cyamids. While there are stories about how Scarback’s wound came to be, it is not known for sure how she was injured. However, what researchers do know is that the wound has not stopped this female from reproducing and successfully raising several calves over her lifetime. After hearing her story from Leigh, I wasn’t surprised that both she and Todd were so thrilled to get both a fecal sample and a drone flight from her early in the season. The two days weren’t all rosy; most of day 1 was shrouded in a cloud of mist resulting in a thin but continuous layer of moisture forming on our clothes, while on day 2 we battled with some pretty big swells (up to 6 feet tall) and in typical Oregon coast style we were victims of a sudden downpour for about 10 minutes. We had some excellent sightings and some not-so-excellent sightings. Sightings where we had four whales surrounding our boat at the same time and sightings where we couldn’t re-locate a whale that had popped up right next to us. It happens.

 

A local celebrity – Scarback. Image captured under NOAA/NMFS permit #21678. Source: Lisa Hildebrand.

 

An ecstatic Lisa with wild hair standing in the bow pulpit of Ruby camera at the ready. Source: Leigh Torres.

Field work is certainly one of my favorite things in the world. The smell of the salt, the rustling of cereal bar wrappers, the whipping of hair, the perpetual rosy noses and cheeks no matter how many times you apply and re-apply sunscreen, the awkward hilarity of clambering onto the back of the boat where the engine is housed to take a potty break, the whooshing sound of a blow, the sometimes gentle and sometimes aggressive rocking of the boat, the realization that you haven’t had water in four hours only to chug half of your water in a few seconds, the waft of peanut butter and jelly sandwiches, the circular footprint where a whale has just gracefully dipped beneath the surface slipping away from view. I don’t think I will ever tire of any of those things.

 

 

More data, more questions, more projects: There’s always more to learn

By Dawn Barlow, PhD student, OSU Department of Fisheries and Wildlife, Geospatial Ecology of Marine Megafauna Lab 

As you may have read in previous blog posts, my research focuses on the ecology of blue whales in New Zealand. Through my MS research and years of work by a dedicated team, we were able to document and describe a population of around 700 blue whales that are unique to New Zealand, present year-round, and genetically distinct from all other known populations [1]. While this is a very exciting discovery, documenting this population has also unlocked a myriad of further questions about these whales. Can we predict when and where the whales are most likely to be? How does their distribution change seasonally? How often do they overlap with anthropogenic activity? My PhD research will aim to answer these questions through models of blue whale distribution patterns relative to their environment at multiple spatial and temporal scales.

Because time at sea for vessel-based surveys is cost-limited and difficult to come by, it is in any scientist’s best interest to collect as many concurrent streams of data as possible while in the field. When Dr. Leigh Torres designed our blue whale surveys that were conducted in 2014, 2016, and 2017, she really did a miraculous job of maximizing time on the water. With more data, more questions can be asked. These complimentary datasets have led to the pursuit of many “side projects”. I am lucky enough to work on these questions in parallel with what will form the bulk of my PhD, and collaborate with a number of people in the process. In this blog post, I’ll give you some short teasers of these “side projects”!

Surface lunge feeding as a foraging strategy for New Zealand blue whales

Most of what we know about blue whale foraging behavior comes from studies conducted off the coast of Southern California[2,3] using suction cup accelerometer tags. While these studies in the California Current ecosystem have led to insights and breakthroughs in our understanding of these elusive marine predators and their prey, they have also led us to adopt the paradigm that krill patches are denser at depth, and blue whales are most likely to target these deep prey patches when they feed. We have combined our prey data with blue whale behavioral data observed via a drone to investigate blue whale foraging in New Zealand, with a particular emphasis on surface feeding as a strategy. In our recent analyses, we are finding that in New Zealand, lunge feeding at the surface may be more than just “snacking”. Rather, it may be an energetically efficient strategy that blue whales have evolved in the region with unique implications for conservation.

Figure 1. A blue whale lunges on an aggregation of krill. UAS piloted by Todd Chandler.

Combining multiple data streams for a comprehensive health assessment

In the field, we collected photographs, blubber biopsy samples, fecal samples, and conducted unmanned aerial system (UAS, a.k.a. “drone”) flights over blue whales. The blubber and fecal samples can be analyzed for stress and reproductive hormone levels; UAS imagery allows us to quantify a whale’s body condition[4]; and photographs can be used to evaluate skin condition for abnormalities. By pulling together these multiple data streams, this project aims to establish a baseline understanding of the variability in stress and reproductive hormone levels, body condition, and skin condition for the population. Because our study period spans multiple years, we also have the ability to look at temporal patterns and individual changes over time. From our preliminary results, we have evidence for multiple pregnant females from elevated pregnancy and stress hormones, as well as apparent pregnancy from the body condition analysis. Additionally, a large proportion of the population appear to be affected by blistering and cookie cutter shark bites.

Figure 2. An example aerial drone image of a blue whale that will be used to asses body condition, i.e. how healthy or malnourished the whale is. (Drone piloted by Todd Chandler).

Figure 3. Images of blue whale skin condition, affected by A) blistering and B) cookie cutter shark bites.

Comparing body shape and morphology between species

The GEMM Lab uses UAS to quantitatively study behavior[5] and health of large whales. From various projects in different parts of the world we have now assimilated UAS data on blue, gray, and humpback whales. We will measure these images to investigate differences in body shape and morphology among these species. We plan to explore how form follows function across baleen whales, based on their different  life histories, foraging strategies, and ecological roles.

Figure 4 . Aerial images of A) a blue whale in New Zealand’s South Taranaki Bight, B) a gray whale off the coast of Oregon, and C) a humpback whale off the coast of Washington. Drone piloted by Todd Chandler (A and B) and Jason Miranda (C). 

So it goes—my dissertation will contain a series of chapters that build on one another to explore blue whale distribution patterns at increasing scales, as well as a growing number of appendices for these “side projects”. Explorations and collaborations like I’ve described here allow me to broaden my perspectives and diversify my analytical skills, as well as work with many excellent teams of scientists. The more data we collect, the more questions we are able to ask. The more questions we ask, the more we seem to uncover that is yet to be understood. So stay tuned for some exciting forthcoming results from all of these analyses, as well as plenty of new questions, waiting to be posed.

References

  1. Barlow DR et al. 2018 Documentation of a New Zealand blue whale population based on multiple lines of evidence. Endanger. Species Res. 36, 27–40. (doi:https://doi.org/10.3354/esr00891)
  2. Hazen EL, Friedlaender AS, Goldbogen JA. 2015 Blue whales (Balaenoptera musculus) optimize foraging efficiency by balancing oxygen use and energy gain as a function of prey density. Sci. Adv. 1, e1500469–e1500469. (doi:10.1126/sciadv.1500469)
  3. Goldbogen JA, Calambokidis J, Oleson E, Potvin J, Pyenson ND, Schorr G, Shadwick RE. 2011 Mechanics, hydrodynamics and energetics of blue whale lunge feeding: efficiency dependence on krill density. J. Exp. Biol. 214, 131–146. (doi:10.1242/jeb.048157)
  4. Burnett JD, Lemos L, Barlow DR, Wing MG, Chandler TE, Torres LG. 2018 Estimating morphometric attributes on baleen whales using small UAS photogrammetry: A case study with blue and gray whales. Mar. Mammal Sci. (doi:10.1111/mms.12527)
  5. 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. (doi:10.3389/fmars.2018.00319)

Photogrammetry Insights

By Leila Lemos, PhD Candidate, Fisheries and Wildlife Department, Oregon State University

After three years of fieldwork and analyzing a large dataset, it is time to finally start compiling the results, create plots and see what the trends are. The first dataset I am analyzing is the photogrammetry data (more on our photogrammetry method here), which so far has been full of unexpected results.

Our first big expectation was to find a noticeable intra-year variation. Gray whales spend their winter in the warm waters of Baja California, Mexico, period while they are fasting. In the spring, they perform a big migration to higher latitudes. Only when they reach their summer feeding grounds, that extends from Northern California to the Bering and Chukchi seas, Alaska, do they start feeding and gaining enough calories to support their migration back to Mexico and subsequent fasting period.

 

Northeastern gray whale migration route along the NE Pacific Ocean.
Source: https://journeynorth.org/tm/gwhale/annual/map.html

 

Thus, we expected to see whales arriving along the Oregon coast with a skinny body condition that would gradually improve over the months, during the feeding season. Some exceptions are reasonable, such as a lactating mother or a debilitated individual. However, datasets can be more complex than we expect most of the times, and many variables can influence the results. Our photogrammetry dataset is no different!

In addition, I need to decide what are the best plots to display the results and how to make them. For years now I’ve been hearing about the wonders of R, but I’ve been skeptical about learning a whole new programming/coding language “just to make plots”, as I first thought. I have always used statistical programs such as SPSS or Prism to do my plots and they were so easy to work with. However, there is a lot more we can do in R than “just plots”. Also, it is not just because something seems hard that you won’t even try. We need to expose ourselves sometimes. So, I decided to give it a try (and I am proud of myself I did), and here are some of the results:

 

Plot 1: Body Area Index (BAI) vs Day of the Year (DOY)

 

In this plot, we wanted to assess the annual Body Area Index (BAI) trends that describe how skinny (low number) or fat (higher number) a whale is. BAI is a simplified version of the BMI (Body Mass Index) used for humans. If you are interested about this method we have developed at our lab in collaboration with the Aerial Information Systems Laboratory/OSU, you can read more about it in our publication.

The plots above are three versions of the same data displayed in different ways. The first plot on the left shows all the data points by year, with polynomial best fit lines, and the confidence intervals (in gray). There are many overlapping observation points, so for the middle plot I tried to “clean up the plot” by reducing the size of the points and taking out the gray confidence interval range around the lines. In the last plot on the right, I used a linear regression best fit line, instead of polynomial.

We can see a general trend that the BAI was considerably higher in 2016 (red line), when compared to the following years, which makes us question the accuracy of the dataset for that year. In 2016, we also didn’t sample in the month of July, which is causing the 2016 polynomial line to show a sharp decrease in this month (DOY: ~200-230). But it is also interesting to note that the increasing slope of the linear regression line in all three years is very similar, indicating that the whales gained weight at about the same rate in all years.

 

Plot 2: Body Area Index (BAI) vs Body Condition Score (BCS)

 

In addition to the photogrammetry method of assessing whale body condition, we have also performed a body condition scoring method for all the photos we have taken in the field (based on the method described by Bradford et al. 2012). Thus, with this second set of plots, we wanted to compare both methods of assessing whale body condition in order to evaluate when the methods agree or not, and which method would be best and in which situation. Our hypothesis was that whales with a ‘fair’ body condition would have a lower BAI than whales with a ‘good’ body condition.

The plots above illustrate two versions of the same data, with data in the left plot grouped by year, and the data in the right plot grouped by month. In general, we see that no whales were observed with a poor body condition in the last analysis months (August to October), with both methods agreeing to this fact. Additionally, there were many whales that still had a fair body condition in August and September, but less whales in the month of October, indicating that most whales gained weight over the foraging seasons and were ready to start their Southbound migration and another fasting period. This result is important information regarding monitoring and conservation issues.

However, the 2016 dataset is still a concern, since the whales appear to have considerable higher body condition (BAI) when compared to other years.

 

Plot 3:Temporal Body Area Index (BAI) for individual whales

 

In this last group of plots, we wanted to visualize BAI trends over the season (using day of year – DOY) on the x-axis) for individuals we measured more than once. Here we can see the temporal patterns for the whales “Bit”, “Clouds”, “Pearl”, “Scarback, “Pointy”, and “White Hole”.

We expected to see an overall gradual increase in body condition (BAI) over the seasons, such as what we can observe for Pointy in 2018. However, some whales decreased their condition, such as Bit in 2018. Could this trend be accurate? Furthermore, what about BAI measurements that are different from the trend, such as Scarback in 2017, where the last observation point shows a lower BAI than past observation points? In addition, we still observe a high BAI in 2016 at this individual level, when compared to the other years.

My next step will be to check the whole dataset again and search for inconsistencies. There is something causing these 2016 values to possibly be wrong and I need to find out what it is. The overall quality of the measured photogrammetry images was good and in focus, but other variables could be influencing the quality and accuracy of the measurements.

For instance, when measuring images, I often struggled with glare, water splash, water turbidity, ocean swell, and shadows, as you can see in the photos below. All of these variables caused the borders of the whale body to not be clearly visible/identifiable, which may have caused measurements to be wrong.

 

Examples of bad conditions for performing photogrammetry: (1) glare and water splash, (2) water turbidity, (3) ocean swell, and (4) a shadow created in one of the sides of the whale body.
Source: GEMM Lab. Taken under NMFS permit 16111 issued to John Calambokidis.

 

Thus, I will need to check all of these variables to identify the causes for bad measurements and “clean the dataset”. Only after this process will I be able to make these plots again to look at the trends (which will be easy since I already have my R code written!). Then I’ll move on to my next hypothesis that the BAI of individual whales varied by demographics including sex, age and reproductive state.

To carry out robust science that produces results we can trust, we can’t simply collect data, perform a basic analysis, create plots and believe everything we see. Data is often messy, especially when developing new methods like we have done here with drone based photogrammetry and the BAI. So, I need to spend some important time checking my data for accuracy and examining confounding variables that might affect the dataset. Science can be challenging, both when interpreting data or learning a new command language, but it is all worth it in the end when we produce results we know we can trust.