A smaller sized gray whale: recent publication finds PCFG whales are smaller than ENP whales

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

A recent blog post by GEMM Lab’s PhD Candidate Clara Bird gave a recap of our 8th consecutive GRANITEfield season this year. In her blog, Clara highlighted that we saw 71 individual gray whales this season, 61 of which we have seen in previous years and identified as belonging to the Pacific Coast Feeding Group (PCFG). With an estimated population size of around 212 individuals, this means that we saw almost 1/3 of the PCFG population this season alone. Since the GEMM Lab first started collecting data on PCFG gray whales in 2016, we have collected drone imagery on over 120 individuals, which is over half the PCFG population. This dataset provides incredible opportunity to get to know these individuals and observe them from year to year as they grow and mature through different life history stages, such as producing a calf. A question our research team has been interested in is what makes a PCFG whale different from an Eastern North Pacific (ENP) gray whale, which has a population size around 16,000 individuals and feed predominantly in the Arctic during the summer months? For this blog, I will highlight findings from our recent publication in Biology Letters (Bierlich et al., 2023) comparing the morphology (body length, skull, and fluke size) between PCFG and ENP populations. 

Body size and shape reflect how an animal functions in their environment and can provide details on an individual’s current health, reproductive status, and energetic requirements. Understanding how animals grow is a key component for monitoring the health of populations and their vulnerability to climate change and other stressors in their environment.  As such, collecting accurate morphological measurements of individuals is essential to model growth and infer their health. Collecting such morphological measurements of whales is challenging, as you cannot ask a whale to hold still while you prepare the tape measure, but as discussed in a previous blog, drones provide a non-invasive method to collect body size measurements of whales. Photogrammetry is a non-invasive technique used to obtain morphological measurements of animals from photographs. The GEMM Lab uses drone-based photogrammetry to obtain morphological measurements of PCFG gray whales, such as their body length, skull length (as snout-to-blowhole), and fluke span (see Figure 1). 

Figure 1. Morphological measurements obtained via photogrammetry of a Pacific Coast Feeding Group (PCFG) gray whale. These measurements were used to compare to individuals from the Eastern North Pacific (ENP) population. 

As mentioned in this previous blog, we use photo-identification to identify unique individual gray whales based on markings on their body. This method is helpful for linking all the data we are collecting (morphology, hormones, behavior, new scarring and skin conditions, etc.) to each individual whale. An individual’s sightings history can also be used to estimate their age, either as a ‘minimum age’ based on the date of first sighting or a ‘known age’ if the individual was seen as a calf. By combining the length measurements from drone-based photogrammetry and age estimates from photo-identification history, we can construct length-at-age growth models to examine how PCFG gray whales grow. While no study has previously examined length-at-age growth models specifically for PCFG gray whales, another study constructed growth curves for ENP gray whales using body length and age estimates obtained from whaling, strandings, and aerial photogrammetry (Agbayani et al., 2020). For our study, we utilized these datasets and compared length-at-age growth, snout-to-blowhole length, and fluke span between PCFG and ENP whales. We used Bayesian statistics to account and incorporate the various levels of uncertainty associated with data collected (i.e., measurements from whaling vs. drone, ‘minimum age’ vs. ‘known age’). 

We found that while both populations grow at similar rates, PCFG gray whales reach smaller adult lengths than ENP. This difference was more extreme for females, where PCFG females were ~1 m (~3 ft) shorter than ENP females and PCFG males were ~0.5 m (1.5 ft) shorter than ENP males (Figure 2, Figure 3). We also found that ENP males and females have slightly larger skulls and flukes than PCFG male and females, respectively. Our results suggest PCFG whales are shaped differently than ENP whales (Figure 3)! These results are also interesting in light of our previous published study that found PCFG whales are skinnier than ENP whales (see this previous blog post). 

Figure 2. Growth curves (von Bertalanffy–Putter) for length-at-age comparing male and female ENP and PCFG gray whales (shading represents 95% highest posterior density intervals). Points represent mean length and median age. Vertical bars represent photogrammetric uncertainty. Dashed horizontal lines represent uncertainty in age estimates.

Figure 3. Schematic highlighting the differences in body size between Pacific Coast Feeding Group (PCFG) and Eastern North Pacific (ENP) gray whales. 

Our results raise some interesting questions regarding why PCFG are smaller: Is this difference in size and shape normal for this population and are they healthy? Or is this difference a sign that they are stressed, unhealthy and/or not getting enough to eat? Larger individuals are typically found at higher latitudes (this pattern is called Bergmann’s Rule), which could explain why ENP whales are larger since they feed in the Arctic. Yet many species, including fish, birds, reptiles, and mammals, have experienced reductions in body size due to changes in habitat and anthropogenic stressors (Gardner et al., 2011). The PCFG range is within closer proximity to major population centers compared to the ENP foraging grounds in the Arctic, which could plausibly cause increased stress levels, leading to decreased growth. 

The smaller morphology of PCFG may also be related to the different foraging tactics they employ on different prey and habitat types than ENP whales. Animal morphology is linked to behavior and habitat (see this blogpost). ENP whales feeding in the Arctic generally forage on benthic amphipods, while PCFG whales switch between benthic, epibenthic and planktonic prey, but mostly target epibenthic mysids. Within the PCFG range, gray whales often forage in rocky kelp beds close to shore in shallow water depths (approx. 10 m) that are on average four times shallower than whales feeding in the Arctic. The prey in the PCFG range is also found to be of equal or higher caloric value than prey in the Arctic range (see this blog), which is interesting since PCFG were found to be skinnier.

It is also unclear when the PCFG formed? ENP and PCFG whales are genetically similar, but photo-identification history reveals that calves born into the PCFG usually return to forage in this PCFG range, suggesting matrilineal site fidelity that contributes to the population structure. PCFG whales were first documented off our Oregon Coast in the 1970s (Figure 4). Though, from examining old whaling records, there may have been PCFG gray whales foraging off the coasts of Northern California to British Columbia since the 1920s.

Figure 4. First reports of summer-resident gray whales along the Oregon coast, likely part of the Pacific Coast Feeding Group. Capital Journal, August 9, 1976, pg. 2.

Altogether, our finding led us to two hypotheses: 1) the PCFG range provides an ecological opportunity for smaller whales to feed on a different prey type in a shallow environment, or 2) the PCFG range is an ecological trap, where individuals gain less energy due to energetically costly feeding behaviors in complex habitat while potentially targeting lower density prey, causing them to be skinnier and have decreased growth. Key questions remain for our research team regarding potential consequences of the smaller sized PCFG whales, such as does the smaller body size equate to reduced resilience to environmental and anthropogenic stressors? Does smaller size effect fecundity and population fitness? Stay tuned as we learn more about this unique and fascinating smaller sized gray whale. 

References

Agbayani, S., Fortune, S. M. E., & Trites, A. W. (2020). Growth and development of North Pacific gray whales (Eschrichtius robustus). Journal of Mammalogy101(3), 742–754. https://doi.org/10.1093/jmammal/gyaa028

Bierlich, K. C., Kane, A., Hildebrand, L., Bird, C. N., Fernandez Ajo, A., Stewart, J. D., Hewitt, J., Hildebrand, I., Sumich, J., & Torres, L. G. (2023). Downsized: gray whales using an alternative foraging ground have smaller morphology. Biology Letters19(8). https://doi.org/10.1098/rsbl.2023.0043

Gardner, J. L., Peters, A., Kearney, M. R., Joseph, L., & Heinsohn, R. (2011). Declining body size: A third universal response to warming? Trends in Ecology and Evolution26(6), 285–291. https://doi.org/10.1016/j.tree.2011.03.005

Title: “Blown away”: measuring the blowholes of whales from drones

By Annie Doron, Undergraduate Intern, Oregon State University, GEMM Laboratory  

Hey up! My name is Annie Doron, and I am an undergraduate Environmental Science student from the University of Sheffield (UK) on my study year abroad. One of my main motivations for undertaking this year abroad was to gain experience working in a marine megafauna lab. Whales in particular have always captivated my interest, and I have been lucky enough to observe  humpback whales in Iceland and The Azores, and even encountered one whilst diving in Australia! For the past 10 months, I have had the unique opportunity to work in the GEMM Lab analyzing Pacific Coast Feeding Group (PCFG) gray whales off the Oregon Coast (Figure 1). I must admit, it has been simply wonderful! 

Figure 1. Aerial image of a PCFG gray whale off the Oregon Coast. 

How did I end up getting involved with the GEMM Lab? I was first accepted into Scarlett Arbuckle’s research-based class in fall term 2022, which is centered around partnering with a mentor for a research project. Having explored the various fields of research at HMSC, I contacted Leigh Torres with interest in getting involved in the GEMM Lab and to establish a research project suitable for a totally inexperienced, international, undergraduate student. Thankfully, Leigh forwarded my email to KC Bierlich who offered to be my mentor for the class, and the rest is history! I first began analyzing drone imagery to measure length and body condition of  PCFG gray whales, which provided an opportunity to get involved with the lab and gain experience using the photogrammetry software MorphoMetriX (Torres & Bierlich, 2020) (see KC’s blog), which is used to make morphometric measurements of whales. Viewing drone imagery of whales sparked my interest in how they use their blowholes (otherwise called ‘nares’) to replenish their oxygen stores; this led to us establishing a research project for the class where we tested if we could use MorphoMetriX to measure blowholes from drone imagery.

Extending this project into winter and spring terms (via research credits) has enabled me to continue working with Leigh and KC, as well as to collaborate with Clara Bird and Jim Sumich. Thanks to KC, who has patiently guided me through the ins and outs of working on a research project, I now feel more confident handling and manipulating large datasets, analyzing drone footage (i.e., differentiating between behavioral states, recording breathing sequences, detecting when a whale is exhaling vs inhaling, etc.), and speaking in public (although I still get pretty bad stage fright, but I think that is a typical conundrum undergrads face). Whatsmore, applying  R – a programming language used for statistical analysis and data visualization, which I have been trying to wrap my head around for years – to my own dataset has helped me greatly enhance my skills using it. 

So, what exciting things have we been working on this year? Given that we often cannot simply study a whale from inside a laboratory – due to size-related logistical implications – we must use proxies (i.e., a variable that is representative of an immeasurable variable). Since cetaceans must return to the surface to offload carbon dioxide and replenish their oxygen stores, measuring their breath frequency and magnitude is one way to study a whale’s oxygen consumption, in turn offering insight into its energy expenditure (Williams, 1999). Blowholes are one proxy we can use to study breath magnitude. Blowholes can be utilized in this way by measuring inhalation duration (the amount of time a whale is inhaling, which is based on a calculation developed by Jim Sumich) and blowhole area (the total area of a blowhole) to gauge variations in tidal volume (the amount of air flowing in and out of the lungs).

Measuring inhalation duration and blowhole area is important because a larger blowhole area (i.e., one that is more dilated) and a longer inhalation duration is indicative of higher oxygen intake, which can infer stress. For example, in this population, higher stress levels are associated with increased vessel traffic (Lemos et al., 2022), and skinnier whales have higher stress levels compared to chubby, healthy whales (Lemos, Olsen, et al., 2022). Hence, measuring the variation around blowholes could be utilized to predict challenges whales face from climate change and anthropogenic disturbance, including fishing (Scordino et al., 2017) and whale watching industry threats (Sullivan & Torres, 2018) (see Clara’s blog), as well as to inform effective management strategies. Furthermore, measuring the variables inhalation duration and blowhole area could help to identify whether whales are taking larger breaths associated with certain ‘gross behavior states’, otherwise known as ‘primary states’, which include: travel, forage, rest, social (Torres et al., 2018). This could enable us to assess the energetic costs of different foraging tactics (i.e., head standing, side-swimming, and bubble blasting (Torres et al., 2018), as well as consequences of disturbance events, on an individual and population health perspective. 

Inhalation duration has been explored in the past by using captive animals. For example, there have been studies on heart rate and breathing of bottlenose dolphins in human care facilities (Blawas et al., 2021; Fahlman et al., 2015). Recently, Nazario et al. (2022) was able to measure inhalation duration and blowhole area using suction-cup video tags. Her study led us to consider if it was possible to measure the parameters and variation around respiration by measuring blowhole area and inhalation duration of PCFGs from drone imagery. We employed MorphoMetriX to study the length, width, and area of a blowhole (Figure 2). Preliminary analyses verified that the areas of the left and right blowholes are very similar (Figure 3); this finding saved us a lot of time because from thereon we only measured either the left or right side. Interestingly, we see some variation in blowhole area within and across individuals (Figure 4). This variation changes within individuals based on primary state. For example, the whales “Glacier”, “Nimbus”, and “Rat” show very little variation whilst traveling but a large amount whilst foraging. Comparatively, “Dice” shows little variation whilst foraging and large variation whilst traveling. Whilst considering cross-individual comparisons, we can see that “Sole”, “Rat”, “Nimbus”, “Heart”, “Glacier”, “Dice”, and “Coal” each exhibit relatively large amounts of variation, yet “Mahalo”, “Luna”, “Harry”, “Hummingbird” and “Batman” exhibit very little. One potential reason for some individuals displaying higher levels of variation than others could be higher levels of exposure to disturbance events that we were unable to measure or evaluate in this study.

Figure 2. How we measured the length, width, and area of a blowhole using MorphoMetriX.

Figure 3. Data driven evidence that the left and the right blowhole areas are very similar. 

Figure 4. Variation in blowhole area amongst individual PCFG whales. The hollow circles represent the means, and the color represents the primary state the whale is exhibiting, foraging (purple) vs. traveling (blue), which will be further explored in Clara’s PhD.

Now, we are venturing into June and are at a stage where we (KC, Clara, Jim, Leigh, and I) are preparing to publish a manuscript! What a way to finish such a fantastic year! The transition from a 3-month-long pilot study to a much larger data analysis and eventual preparation for a manuscript has been a monumental learning experience. If anybody had told me a year ago that I would be involved in publishing a body of work – especially one that is so meaningful to me – I would simply not have believed them! We hope this established methodology for measuring blowholes will help other researchers carry out blowhole measurements using drone imagery across different populations and species. Further research is required to explore the differences in inhalation duration and blowhole area between different primary states, specifically across different foraging tactics.

It has been a great privilege working with the GEMM Lab these past months, and I was grateful to be included in their monthly lab meetings, during which members gave updates and we discussed recently published papers. Seeing such an enthusiastic, kind, and empathic group of people working together taught me what working in a supportive lab could look and feel like. In spite of relocating from Corvallis to Bend after my first term, I was happy to be able to continue working remotely for the lab for the remainder of my time (even though I was ~200 miles inland). I thoroughly enjoyed living in Corvallis, highlights of which were scuba diving adventures to the Puget Sound and coastal road trips with friends. The appeal to move arose from Bend’s reputation as an adventure hub – with unlimited opportunities for backcountry ski access – as well as its selection of wildlife ecology courses (with a focus on species specific to central Oregon). I moved into ‘Bunk & Brew’ (Bend’s only hostel, which is more like a big house of friends with occasional hostel guests) on January 1st after returning from spending Christmas with friends in my old home in Banff, Canada. I have since been enjoying this wonderful multifaceted lifestyle; working remotely in the GEMM Lab, attending in-person classes, working part-time at the hostel, as well as skiing volcanoes (Mount Hood, Middle and South Sister (Figure 5) or climbing at Smith Rock during my days off. Inevitably, I do miss the beautiful Oregon coast, and I will always be grateful for this ideal opportunity and hope this year marks the start of my marine megafauna career!

Figure 5. What I get up to when I’m not studying blowholes! (This was taken at 5am on the long approach to Middle and North Sister. North Sister is the peak featured in the backdrop).

References

Blawas, A. M., Nowacek, D. P., Allen, A. S., Rocho-Levine, J., & Fahlman, A. (2021). Respiratory sinus arrhythmia and submersion bradycardia in bottlenose dolphins (Tursiops truncatus). Journal of Experimental Biology, 224(1), jeb234096. https://doi.org/10.1242/jeb.234096

Fahlman, A., Loring, S. H., Levine, G., Rocho-Levine, J., Austin, T., & Brodsky, M. (2015). Lung mechanics and pulmonary function testing in cetaceans. Journal of Experimental Biology, 218(13), 2030–2038. https://doi.org/10.1242/jeb.119149

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), 18580. https://doi.org/10.1038/s41598-022-14510-5

Lemos, L. S., Olsen, A., Smith, A., Burnett, J. D., Chandler, T. E., Larson, S., Hunt, K. E., & Torres, L. G. (2022). Stressed and slim or relaxed and chubby? A simultaneous assessment of gray whale body condition and hormone variability. Marine Mammal Science, 38(2), 801–811. https://doi.org/10.1111/mms.12877

Nazario, E. C., Cade, D. E., Bierlich, K. C., Czapanskiy, M. F., Goldbogen, J. A., Kahane-Rapport, S. R., van der Hoop, J. M., San Luis, M. T., & Friedlaender, A. S. (2022). Baleen whale inhalation variability revealed using animal-borne video tags. PeerJ, 10, e13724. https://doi.org/10.7717/peerj.13724

Scordino, J., Carretta, J., Cottrell, P., Greenman, J., Savage, K., & Scordino, J. (2017). Ship Strikes and Entanglements of Gray Whales in the North Pacific Ocean. Cambridge: International Whaling Commission, 1924–2015.

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

Sumich, J. L. (1994). Oxygen extraction in free-swimming gray whale caves. Marine Mammal Science, 10(2), 226–230. https://doi.org/10.1111/j.1748-7692.1994.tb00266.x

Torres, W., & Bierlich, K. (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

Torres, L. G., Nieukirk, S. L., Lemos, L., & Chandler, T. E. (2018). Drone Up! Quantifying Whale Behavior From a New Perspective Improves Observational Capacity. Frontiers in Marine Science, 5, 319. https://doi.org/10.3389/fmars.2018.00319
Williams, T. M. (1999). The evolution of cost efficient swimming in marine mammals: Limits to energetic optimization. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 354(1380), 193–201. https://doi.org/10.1098/rstb.1999.0371

So big, but so small: why the smallest of the largest whales are not smaller

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

Baleen whales are known for their gigantism and encompass a wide range in body sizes extending from blue whales that are the largest animals to live on earth (max length ~30 m) to minke whales (max length ~10 m) that are the smallest of baleen whales (Fig. 1). While all baleen whales are filter feeders, a group called the rorquals use a feeding strategy known as lunge feeding (or intermittent engulfment filtration), which involves engulfing large volumes of prey-laden water at high speeds and then filtering the water out of their mouth using their baleen as a “sieve”. There is positive allometry associated with this feeding technique and body size, meaning that as whales are larger, this feeding strategy becomes more efficient due to increased engulfment of water volume per each lunge feeding event. In other words, a bigger body size equates to a much larger mouthful of food. For example, a minke whale (body length ~7-10 m) will engulf water volume equivalent to ~42% of its body mass, while a blue whale (~21-24 m) engulfs ~135%. Thus, filter feeding enables gigantism through efficient exploitation of large, dense patches of prey. An interesting question then arises: what is the minimum body size at which filter feeding is still efficient? Or in other words, why are the smallest of the baleen whales, minke whales, not smaller? For this blog, I will highlight a study published today in Nature Ecology and Evolution titled “Minke whale feeding rate limitations suggest constraints on the minimum body size for engulfment filtration feeding” led by friend and collaborator of the GEMM Lab Dr. Dave Cade and included myself and other collaborators as co-authors from Stanford University, UC Santa Cruz, Cascadia Research Collective, Duke University, and University of Queensland.

Figure 1. Aerial imagery collected using drones of several baleen whales of various sizes. Each species shown is considered a rorqual whale, except for gray whales. Figure from Segre et al. (2022)

The largest animals of today are marine filter feeders, such as whale sharks, manta rays, and baleen whales, which all share parallel evolutionary histories in which their large body sizes and filter-feeding morphologies are derived from smaller-bodied ancestors that targeted single prey items. Changes in ocean productivity increased the concentrations of smaller prey in the oceans around 5 million years ago, enabling filter feeding as an efficient feeding strategy through capture of abundant aggregations of prey by filtering large volumes of water. It is interesting to note, that within these filter feeding lineages of animals, there are groups of animals that are single-prey foragers with smaller body sizes. For example, the whale shark is the only filter feeder amongst the carpet sharks and the manta ray is much larger than other rays that feed on single prey items. Amongst cetaceans, the smallest single-prey foragers, dolphins (~2-3 m) and porpoises (~1.4-1.9 m), are much smaller than the smallest of the filter feeding cetaceans, minke whales (~7-10 m). These common differences in body sizes and feeding strategies within lineages suggest that there may be minimum body size requirements for this filter feeding strategy to be efficient.

To investigate the limits on minimum body size for filter feeding, our study explored the foraging behavior of Antarctic minke whales, the smallest of the rorqual baleen whales, along the Western Antarctic Peninsula. Our team tagged a total of 23 individuals using non-invasive suction cup tags, like the ones we use for our tagging component in the GEMM Lab’s GRANITE project (see this blog for more details). One of my roles on the project was to obtain aerial imagery of the minke whales using drones to obtain body length measurements (sound familiar?) (Figs. 2-4). Flying drones in Antarctica over minke whales was an amazing experience. The minke whales were often found deep within the bays amongst ice floes and brash ice where they can be very tricky to spot, as they’ll often surface and then quickly disappear, hence their nickname “sneaky minkes”. They also appear “playful” and “athletic” as they are incredibly quick and maneuverable, doing barrel rolls and quick bank turns while they swim. Check out my past blog to read more on accounts of flying over these amazing whales.

Figure 2. Drone image of our team about to place a noninvasive suction cup biologging tag on an Antarctic minke whale. Photo credit: Duke University Marine Robotics and Remote Sensing Lab.
Figure 3. A drone image of a newly tagged and curious Antarctic minke whale approaching our research team. Photo credit: Duke University Marine Robotics and Remote Sensing Lab.
Figure 4. A drone image of a group of Antarctic minke whales swimming through the icy waters along the Antarctic Peninsula. Photo credit: Duke University Marine Robotics and Remote Sensing Lab.

In total, our team collected 437 hours of tag data consisting of day- and night-time foraging behaviors. While the proportion of time spent foraging and the number of lunges per dive (~3-4) was similar between day- and night-time foraging, daytime foraging was much deeper (~72 m) compared to nighttime foraging (~28 m) due to vertical migration of Antarctic krill, their main food source. Overall, nighttime foraging was much more intense than daytime foraging, with an average of 165 lunges per hour during the night compared to 53 lunges per hour during the day. These shallower nighttime dives enabled quicker surface sequences for replenishing oxygen reserves to then return to foraging, whereas the deeper dives during the day required longer surface recovery times before beginning another foraging dive. Thus, nighttime dives are a more efficient and critical component of minke whale foraging.

When it comes to body size, there was no relationship between dive depth and dive duration with body length, except for daytime deep dives, where longer minke whales dove for longer periods than smaller whales. These longer dive times also require longer surface times to replenish oxygen reserves. Longer minke whales can gulp larger amounts of food and thus need longer filtration times to process water from each engulfment. For example, a 9 m minke whale will take 50% longer to filter water through its baleen compared to a 5 m minke whale. In turn, smaller minke whales would need to feed more frequently than larger minke whales in order to maintain efficient foraging. This decreasing efficiency with smaller body size shines light on a broader trend for filter feeders that we refer to in our study as the minimum-size constraint (MSC) hypothesis: “while the maximum size of a filter-feeding body plan will be restricted by physical properties, the minimum size is restricted by the energetic efficiency of filter feeding and the time required to extract sufficient particles from the water” (Cade et al. 2023). When we examined the scaling of maximum feeding rates of minke whales, we found evidence of a minimum size constraint on efficiency at lengths around 5 m. Interestingly, the weaning length of minke whales is reported to be 4.5 – 5.5 m. Before weaning, newborn/yearling minke whales that are smaller than 4.5 ­– 5.5 m have a different foraging strategy where they are dependent on maternal milk. Thus, it is likely that the body size at weaning is influenced by the minimum size at which this specialized foraging technique of lunge feeding becomes efficient.

This study helps inform the evolutionary pathway for filter feeding whales and suggests that efficient filter feeding and gigantism likely co-evolved within the last 5 million years when ocean conditions changed to support larger prey patches suitable for lunge feeding. It is interesting to think about the MSC hypothesis for other baleen whale species that employ alternative filter feeding techniques, such as gray whales that generally use a form of filter feeding called suction feeding. Gray whales are estimated to have a birth length of ~4.6 m (Agbayani et al., 2020), and the body length of newly weaned calves that we have observed along the Oregon Coast from drone imagery seem to be ~8 – 9 m. Perhaps this is the minimum size of when suction feeding becomes efficient for a gray whale? This is something the GEMM Lab hopes to further explore as we continue to collect foraging data from suction cup tags and behavior and body size measurements from drone imagery.

References

Agbayani, S., Fortune, S. M., & Trites, A. W. (2020). Growth and development of North Pacific gray whales (Eschrichtius robustus). Journal of Mammalogy101(3), 742-754.

Cade, D.E., Kahane-Rapport, S.R., Gough, W.T., Bierlich, K.C., Linksy, J.M.J., Johnston, D.W., Goldbogen, J.A., Friedlaender, A.S. (2023). Ultra-high feeding rates of Antarctic minke whales imply a lower limit for body size in engulfment filtration feeders. Nature Ecology and Evolution. https://www.nature.com/articles/s41559-023-01993-2  

Paolo S. Segre, William T. Gough, Edward A. Roualdes, David E. Cade, Max F. Czapanskiy, James Fahlbusch, Shirel R. Kahane-Rapport, William K. Oestreich, Lars Bejder, K. C. Bierlich, Julia A. Burrows, John Calambokidis, Ellen M. Chenoweth, Jacopo di Clemente, John W. Durban, Holly Fearnbach, Frank E. Fish, Ari S. Friedlaender, Peter Hegelund, David W. Johnston, Douglas P. Nowacek, Machiel G. Oudejans, Gwenith S. Penry, Jean Potvin, Malene Simon, Andrew Stanworth, Janice M. Straley, Andrew Szabo, Simone K. A. Videsen, Fleur Visser, Caroline R. Weir, David N. Wiley, Jeremy A. Goldbogen; Scaling of maneuvering performance in baleen whales: larger whales outperform expectations. J Exp Biol 1 March 2022; 225 (5): jeb243224. doi: https://doi.org/10.1242/jeb.243224

How fat do baleen whales get? Recent publication shows how humpback whales increase their body condition over the foraging season. 

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

Traveling across oceans takes a lot of energy. Most baleen whales use stored energy acquired on their summer foraging grounds to support the costs of migration to and reproduction on their winter breeding grounds. Since little, if any, feeding takes place during the migration and winter season, it is essential that baleen whales obtain enough food to increase their fat reserves to support reproduction. As such, baleen whales are voracious feeders, and they typically depart the foraging grounds much fatter than when they had arrived. 

So, how fat do baleen whales typically get by the end of the foraging season, and how does this differ across reproductive classes, such as a juvenile female vs. a pregnant female? Understanding these questions is key for identifying what a typical “healthy” whale looks like, information which can then help scientists and managers monitor potential impacts from environmental and anthropogenic stressors. In this blog, I will discuss a recent publication in Frontiers in Marine Science (https://doi.org/10.3389/fmars.2022.1036860) that is from my PhD dissertation with the Duke University Marine Robotics and Remote Sensing (MaRRS) Lab, and also includes GEMM lab members Allison Dawn and Clara Bird. In this study, we analyzed how humpback whales (Megaptera novaeangliae) along the Western Antarctic Peninsula (WAP) increase their fat reserves throughout the austral summer foraging season (Bierlich et al., 2022). This work also helps provide insight to the GEMM Lab’s GRANITE project (Gray whale Response to Ambient Noise Informed by Technology and Ecology), where we are interested in how Pacific Coast Feeding Group (PCFG) gray whales increase their energy reserves in response to environmental variability and increasing human activities. 

Eastern South Pacific humpback whales, identified as Stock G by the International Whaling Commission, travel over 16,000 km between summer foraging grounds along the WAP and winter breeding grounds between Ecuador and Costa Rica (Fig. 1). Like most baleen whales, Stock G humpback whales were heavily exploited by 20th century commercial whaling. Recent evidence suggests that this population is recovering, with an estimated increase in population size of ~7,000 individuals in 2000 to ~19,107 in 2020 (Johannessen et al., 2022). 

However, there are long-term concerns for this population. The WAP is one of the fastest warming regions on the planet, and regional populations of krill, an important food source for humpback whales, have declined steeply over the past half-century. Additionally, the WAP has seen a rapid expansion of human activities, such as tourism and krill fishing. Specifically, the WAP has experienced an increase in tourism from a total of 6,700 visitors from 59 voyages in 1990 to 73,000 visitors from 408 voyages in 2020, which may be causing increased stress levels amongst Stock G (Pallin et al., 2022). Furthermore, the krill fishery has increased harvest activities in key foraging areas for humpback whales (Reisinger et al., 2022). Understanding how humpback whales increase their energy reserves over the course of the foraging season can help researchers establish a baseline to monitor future impacts from climate change and human activities. This work also provides an opportunity for comparisons to other baleen whale populations that are also exposed to multiple stressors, such as the PCFG gray whales off the Newport Coast who are constantly exposed to vessel traffic and at risk of entanglement from fishing gear. 

Figure 1. The migration route of the Stock G humpback whale population. Figure adapted from Whales of the Antarctic Peninsula Report, WWF 2018.

To understand how humpback whales increase their energy reserves throughout the foraging season, we collected drone imagery of whales along the WAP between November and June, 2017-2019 (Fig. 2). We used these images to measure the length and width of the whale to estimate body condition, which represents an animal’s relative energy reserve and can reflect foraging success (see previous blog). We collected drone imagery from a combination of research stations (Palmer Station), research vessels (Laurence M. Gould), and tour ships (One Ocean Expeditions). We used several different drones types and accounted for measurement uncertainty associated with the camera, focal length lens, altitude, and altimeter (barometer/LiDAR) from each drone (see previous blog and Bierlich et al., 2021a, 2021b). We also took biopsy samples to identify the sex of each individual and to determine if females were pregnant or not. 

Figure 2. Two humpbacks gracefully swimming in the chilly water along the Western Antarctic Peninsula. Photo taken by KC Bierlich & the Duke University Marine Robotics and Remote Sensing (MaRRS) Lab.

Our final dataset included body condition measurements for 228 total individuals. We found that body condition increased linearly between November and June for each reproductive class, which included calves, juvenile females, juvenile whales of unknown sex, lactating females, mature whales of unknown sex, and non-pregnant females (Fig. 3). This was an interesting finding because a recent publication analyzing tagged whales from the same population found that humpback whales have high foraging rates in early season that then significantly decrease by February and March (Nichols et al., 2022). So, despite these reduced foraging rates throughout the season, humpback whales continue to gain substantial mass into the late season. This continued increase in body condition implies a change in krill abundance and/or quality into the late season, which may compensate for the lower feeding rates. For example, krill density and biomass increases by over an order of magnitude across the season (Reiss et al., 2017) and their lipid content increases by ~4x (Hagen et al., 1996). Thus, humpback whales likely compensate for their lower feeding rates by feeding on denser and higher quality krill, ultimately increasing their efficiency in energy deposition. 

Figure 3. Body condition, here measured as Body Area Index (BAI), increases linearly for each reproductive class across the austral summer foraging season (Nov – June) for humpback whales along the Western Antarctic Peninsula. The shading represents the uncertainty around the estimated relationship. The colors represent the month of data collection.

We found that body condition increase varied amongst reproductive classes. For example, lactating females had the poorest measures of body condition across the season, reflecting the high energetic demands of nursing their calves (Fig. 3). Conversely, non-pregnant females had the highest body condition at the start of the season compared to all the other classes, likely reflecting the energy saved and recovered by skipping breeding that year.  Calves, juvenile whales, and mature whales all reached similar levels of body condition by the end of the season, though mature whales will likely invest most of their energy stores toward reproduction, whereas calves and juveniles likely invest toward growth. We also found a positive relationship between the total length of lactating females and their calves, suggesting that bigger moms have bigger calves (Fig. 4). A similar trend has also been observed in other baleen whale species including southern and North Atlantic right whales (Christiansen et al., 2018; Stewart et al., 2022).

Figure 4. Big mothers have big calves. Total length (TL) measurement between mother-calf pairs. The bars around each point represents the uncertainty (95% highest posterior density intervals). The colors represent the month of data collection. The blue line represents the best fit from a Deming regression, which incorporate measurement uncertainty in both the independent (mother’s TL) and dependent variable (calf’s TL).

The results from the humpback study provide insight for my current work exploring how PCFG gray whales increase their energy reserves in relation to environmental variability and increasing human activities. Over the past seven years, the GEMM Lab has been collecting drone images of PCFG gray whales off the coast of Oregon to measure their body condition (see this GRANITE Project blog). Many of the individuals we encounter are seen across years and throughout the foraging season, providing an opportunity to evaluate how an individual’s body condition is influenced by environmental variation, stress levels, maturity, and reproduction. For example, we had nine total body condition measurements of a female PCFG whale named “Sole”, who had a curvilinear increase in body condition throughout the summer foraging season – a rapid increase in early season that slowed as the season progressed (Fig. 5). This raises many questions for us: is this how most PCFG whales typically increase their body condition during the summer? Is this increase different for pregnant or lactating females? How is this increase impacted by environmental variability or anthropogenic stressors? Repeated measurements of individuals, in addition to Sole, in different reproductive classes across different years will help us determine what body condition is considered a healthy range for gray whales. This is particularly important for monitoring any potential health consequences from anthropogenic stressors, such as vessel noise and traffic (see recent blog by GEMM Lab alum Leila Lemos). We are currently analyzing body condition measurements between 2016 – 2022, so stay tuned for upcoming results!

Figure 6. Body condition, here measured as Body Area Index (BAI), increases curvilinearly for “Sole”, a mature female Pacific Coat Feeding Group gray whale, imaged nine times along the Oregon coast in 2021. The colors represent the month of data collection. 

References

Bierlich, K. C., Hewitt, J., Bird, C. N., Schick, R. S., Friedlaender, A., Torres, L. G., et al. (2021a). Comparing Uncertainty Associated With 1-, 2-, and 3D Aerial Photogrammetry-Based Body Condition Measurements of Baleen Whales. Front. Mar. Sci. 8, 1–16. doi:10.3389/fmars.2021.749943.

Bierlich, K. C., Hewitt, J., Schick, R. S., Pallin, L., Dale, J., Friedlaender, A. S., et al. (2022). Seasonal gain in body condition of foraging humpback whales along the Western Antarctic Peninsula. Front. Mar. Sci. 9, 1–16. doi:10.3389/fmars.2022.1036860.

Bierlich, K., Schick, R., Hewitt, J., Dale, J., Goldbogen, J., Friedlaender, A., et al. (2021b). Bayesian approach for predicting photogrammetric uncertainty in morphometric measurements derived from drones. Mar. Ecol. Prog. Ser. 673, 193–210. doi:10.3354/meps13814.

Christiansen, F., Vivier, F., Charlton, C., Ward, R., Amerson, A., Burnell, S., et al. (2018). Maternal body size and condition determine calf growth rates in southern right whales. Mar. Ecol. Prog. Ser. 592, 267–281.

Hagen, W., Van Vleet, E. S., and Kattner, G. (1996). Seasonal lipid storage as overwintering strategy of Antarctic krill. Mar. Ecol. Prog. Ser. 134, 85–89. doi:10.3354/meps134085.

Johannessen, J. E. D., Biuw, M., Lindstrøm, U., Ollus, V. M. S., Martín López, L. M., Gkikopoulou, K. C., et al. (2022). Intra-season variations in distribution and abundance of humpback whales in the West Antarctic Peninsula using cruise vessels as opportunistic platforms. Ecol. Evol. 12, 1–13. doi:10.1002/ece3.8571.

Nichols, R., Cade, D. E., Kahane-Rapport, S., Goldbogen, J., Simpert, A., Nowacek, D., et al. (2022). Intra-seasonal variation in feeding rates and diel foraging behavior in a seasonally fasting mammal, the humpback whale. Open Sci. 9, 211674.

Pallin, L. J., Botero-Acosta, N., Steel, D., Baker, C. S., Casey, C., Costa, D. P., et al. (2022). Variation in blubber cortisol levels in a recovering humpback whale population inhabiting a rapidly changing environment. Sci. Rep. 12, 1–13. doi:10.1038/s41598-022-24704-6.

Reisinger, R., Trathan, P. N., Johnson, C. M., Joyce, T. W., Durban, J. W., Pitman, R. L., et al. (2022). Spatiotemporal overlap of baleen whales and krill fisheries in the Antarctic Peninsula region. Front. Mar. Sci. doi:doi: 10.3389/fmars.2022.914726.

Reiss, C. S., Cossio, A., Santora, J. A., Dietrich, K. S., Murray, A., Greg Mitchell, B., et al. (2017). Overwinter habitat selection by Antarctic krill under varying sea-ice conditions: Implications for top predators and fishery management. Mar. Ecol. Prog. Ser. 568, 1–16. doi:10.3354/meps12099.

Stewart, J. D., Durban, J. W., Europe, H., Fearnbach, H., Hamilton, P. K., Knowlton, A. R., et al. (2022). Larger females have more calves : influence of maternal body length on fecundity in North Atlantic right whales. Mar. Ecol. Prog. Ser. 689, 179–189. doi:10.3354/meps14040.

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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References

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

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

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

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

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

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

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

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

The many dimensions of a fat whale: Using drones to measure the body condition of baleen whales 

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

In my last blog, I discussed how to obtain morphological measurements from drone-based imagery of whales and the importance of calculating and considering uncertainty, as different drone platforms have varying levels of measurement uncertainty. But how does uncertainty scale and propagate when multiple measurements are combined, such as when measuring body condition of the whole animal? In this blog, I will discuss the different methods used for measuring body condition of baleen whales from drone-based imagery and how uncertainty differs between these metrics.

Body condition is defined as the energy stored in the body as a result of feeding and is assumed to indicate an animal’s overall health, as it reflects the balance between energy intake and investment toward growth, maintenance and reproduction (Peig and Green, 2009). Thus, body condition reflects the foraging success of an individual, as well as the potential for reproductive output and the quality of habitat. For example, female North American brown bears (Ursus arctos) in high quality habitats were in better body condition, produced larger litter sizes, and lived in greater population densities compared to females in lower quality habitats (Hilderbrand et al., 1999). As Dawn Barlow and Will Kennerley discussed in their recent blog, baleen whales are top predators and serve as ecosystem sentinels that shed light not only on the health of their population, but on the health of their ecosystem. As ocean climate conditions continue to change, monitoring the body condition of baleen whales is important to provide insight on how their population and ecosystem is responding. 

As discussed in a previous blog, drones serve as a valuable tool for obtaining morphological measurements of baleen whales to estimate their body condition. Images are imported into photogrammetry software, such as MorphoMetriX (Torres and Bierlich, 2020), to measure the total length of an individual and that is then divided into perpendicular width segments (i.e., in 5 or 10% increments) down the body (Fig. 1). These total length and width measurements are then used to estimate body condition in either 1-, 2-, or 3-dimensions: a single width (1D), a projected dorsal surface area (2D), or a body volume measure (3D). These 1D, 2D, and 3D measurements of body condition can then be standardized by total length to produce a relative measure of an individual’s body condition to compare among individuals and populations. 

Figure 1. An example of a Pacific Coast Feeding Group (PCFG) gray whale measured in MorphoMetriX (Torres & Bierlich, 2020).

While several different studies have used each of these dimensions to assess whale body condition, it is unclear how these measurements compare amongst each other. Importantly, it is also unclear how measurement uncertainty scales across these multiple dimensions and influences inference, which can lead to misinterpretation of data. For example, the surface area and volume of two geometrically similar bodies of different sizes are not related to their linear dimensions in the same ratio, but rather to the second and third power, respectively (i.e., x2 vs. x3).  Similarly, uncertainty should not be expected to scale linearly across 1D, 2D, and 3D body condition measurements. 

The second chapter of my dissertation, which was recently published in Frontiers in Marine Science and includes Clara Bird and Leigh Torres as co-authors, compared the uncertainty associated with 1D, 2D, and 3D drone-based body condition measurements in three baleen whale species with different ranges in body sizes: blue, humpback, and Antarctic minke whales (Figure 2) (Bierlich et al., 2021). We used the same Bayesian model discussed in my last blog, to incorporate uncertainty associated with each 1D, 2D, and 3D estimate of body condition. 

Figure 2. An example of total length and perpendicular width (in 5% increments of total length) measurements of an individual blue, humpback and Antarctic minke whale. Each image measured using MorphoMetriX (Torres and Bierlich, 2020). 

We found that uncertainty does not scale linearly across multi-dimensional measurements, with 2D and 3D uncertainty increasing by a factor of 1.45 and 1.76 compared to 1D, respectively. This result means that there is an added cost of increased uncertainty when utilizing a multidimensional body condition measurement. Our finding is important to help researchers decide which body condition measurement best suits their scientific question,  particularly when using a drone platform that is susceptible to greater error – as discussed in my previous blog. However, a 1D measurement only relies on a single width measurement, which may be excluding other regions of an individual’s body condition that is important for energy storage. In these situations, a 2D or 3D measure may be more appropriate.

We found that when comparing relative measures of body condition (standardized by total length of the individual), each standardized metric was highly correlated with one another. This finding suggests that 1D, 2D, and 3D metrics will draw similar relative predictions of body condition for individuals, allowing researchers to be confident they will draw similar conclusions relating to the body condition of individuals, regardless of which standardized metric they use. However, when comparing the precision of each of these metrics, the body area index (BAI) – a 2D standardized metric – displayed the highest level of precision. This result highlights how BAI can advantageously detect small changes in body condition, which is useful for comparing individuals or even tracking the same individual over time.

BAI was developed by the GEMM Lab (Burnett et al., 2018) and was designed to be similar to body mass index (BMI) in humans [BMI = mass (kg)/(height (m))2], where BAI uses the calculated surface area as a surrogate for body mass. In humans, a healthy BMI range is generally considered 18.5–24.9, below 18.5 is considered underweight, above 24.9 is considered overweight, and above 30 is considered obese (Flegal et al., 2012). Identifying a healthy range in BAI for baleen whales is challenged by a limited knowledge of what a “healthy” body condition range is for a whale. We found strong evidence that a healthy range of BAI is species-specific, as each species displayed a distinctive range in BAI: blue whales: 11–16; AMW: 17–24; humpback whales: 23–32; humpback whale calves: 23–28 (Fig. 3). These differences in BAI ranges likely reflect differences in the body shape of each species (Fig. 4). For example, humpbacks have the widest range of BAI compared to these other two species, which was also reflected in their larger variation in perpendicular widths (Figs. 2-4). Thus, it seems that BAI offers conditionally “scalefree” comparisons between species, yet it is unreasonable to set a single, all-whale BAI threshold to determine “healthy” versus “unhealthy” body condition.  Collecting a large sample of body condition measurements across many individuals and demographic units over space and time with information on vital rates (e.g., reproductive capacity) will help elucidate a healthy BAI range for each species.

Figure 3. Body area index (BAI) for each species. AMW = Antarctic minke whale.  Figure from Bierlich et al. (2021).
Figure 4. A) Absolute widths (m) and B) relative widths, standardized by total length (TL) to help elucidate the different body shapes of Antarctic minke whales (AMW; n = 40), blue whales (n = 32), humpback whales (n = 40), and humpback whale calves (n = 15). Note how the peak in body width occurs at a different percent body width between species, demonstrating the natural variation in body shape between baleen whales. Figure from Bierlich et al. (2021).

Over the past six years, the GEMM Lab has been collecting drone images of Pacific Coast Feeding Group (PCFG) gray whales off the coast of Oregon to measure their BAI (see GRANITE Project blog). Many of the individuals we encounter are seen across years and throughout the foraging season, providing an opportunity to evaluate how an individual’s BAI is influenced by environmental variation, stress levels, maturity, and reproduction. These data will in turn help determine what the healthy range in BAI for gray whales is. For example, linking BAI to pregnancy – whether a whale is currently pregnant or becomes pregnant the following season – will help determine what BAI is needed to support calf production. We are currently analyzing hundreds of body condition measurements from 2016 – 2021, so stay tuned for upcoming results!

References

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

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

Flegal, K. M., Carroll, M. D., Kit, B. K., & Ogden, C. L. (2012). Prevalence of Obesity and Trends in the Distribution of Body Mass Index Among US Adults, 1999-2010. JAMA307(5), 491. https://doi.org/10.1001/jama.2012.39

Hilderbrand, G. V, Schwartz, C. C., Robbins, C. T., Jacoby, M. E., Hanley, T. A., Arthur, S. M., & Servheen, C. (1999). The importance of meat, particularly salmon, to body size, population productivity, and conservation of North American brown bears. Canadian Journal of Zoology77(1), 132–138.

Peig, J., & Green, A. J. (2009). New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos118(12), 1883–1891.

Torres, W., & Bierlich, K. C. (2020). MorphoMetriX: a photogrammetric measurement GUI for morphometric analysis of megafauna. Journal of Open Source Software5(45), 1825–1826.

Drones with lasers: almost as cool as “sharks with laser beams attached to their heads”

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

The recent advancement in drones (or unoccupied aircraft systems, UAS) has greatly enhanced opportunities for scientists across a broad range of disciplines to collect high-resolution aerial imagery. Wildlife researchers in particular have utilized this technology to study large elusive animals, such as whales, to observe their behavior (see Clara Bird’s blog) and obtain morphological measurements via photogrammetry (see previous blog for a brief history on photogrammetry and drones). However, obtaining useful measurement data is not as easy as flying the drone and pressing record. For this blog, I will provide a brief overview on the basics of using photogrammetry to extract morphological measurements from images collected with drones, as well as the associated uncertainty from using different drone platforms. 

During my PhD at Duke University, I co-developed an open-source photogrammetry software called MorphoMetriX to measure whales in images I collected using drones (Fig. 1) (Torres and Bierlich, 2020) (see this blog for some fieldwork memoirs!). The software is designed to be flexible, simple to use, and customizable without knowledge of scripting languages. Using MorphoMetriX, measurements are made in pixels and then multiplied by the ground sampling distance (GSD) to convert to standard units (e.g., meters) (Fig. 2A). GSD represents the distance on the ground each pixel represents (i.e., the linear size of the pixel) and therefore sets the scale of the image (i.e., cm per pixel). Figure 2A describes how GSD is dependent on the camera sensor, focal length lens, and altitude. Thus, drones equipped with different cameras and focal length lenses will have inherent differences in GSD as altitude increases (Fig. 2B). A larger GSD increases the length each pixel represents in a photo and results in a lower resolution image, potentially obscuring important features in the photo and introducing measurement error.

Figure 1. An example of a Pacific Coast Feeding Group gray whale measured in MorphoMetriX (Torres & Bierlich, 2020).
Figure 2: Overview of photogrammetry methods and calculating ground sampling distance (GSD). A) Photogrammetry methods for how each image is scaled to convert measurements in pixels to standard units (e.g., meters). Altitude is the distance between the camera lens and whale (usually at the surface of the water). Figure from Torres and Bierlich (2020). B) The exact (not accounting for distortion or altitude error) ground sampling distance (GSD) for two drone platforms commonly used to obtain morphological measurements of cetaceans. The difference in GSD between the P4Pro and Inspire 1 is due to the difference in sensor width and focal lengths of the cameras used. Figure from Bierlich et al. (2021).

Obtaining accurate altitude information is a key component in obtaining accurate measurements. All drones are equipped with a barometer, which measures altitude from changes in pressure. In general, barometers usually yield low accuracy in the altitude recorded, particularly for low-cost sensors commonly found on small, off-the-shelf drones (Wei et al., 2016). Dawson et al. (2017) added a laser altimeter (i.e., LightWare SF11/C, https://www.mouser.com//datasheet//2//321//28054-SF11-Laser-Altimeter-Manual-Rev8-1371857.pdf) to a drone, which yields higher accuracy in the altitude recorded. Since then, several studies have adopted use of a laser altimeter to study different species of baleen whales (i.e., Gough et al., 2019; Christiansen et al., 2018).

The first chapter of my dissertation, which was published last year in Marine Ecology Progress Series, compared the accuracy of several drones equipped with different camera sensors, focal length lenses, and a barometer vs. laser altimeter (Bierlich et al., 2021). We flew each drone over a known sized object floating at the surface and collected images at various altitudes (between 10 – 120 m). We used the known size of the floating object to determine the percent error of each measurement at each altitude. We found that 1) there is a lot of variation in measurement error across the different drones when using a barometer to measure altitude and 2) using a laser altimeter dramatically reduces measurement error for each drone (Fig. 3).

Figure 3. The % error for measurements from different drones. Black dashed line represents 0% error (true length = 1.48 m). The gray dashed lines represent under- and over-estimation of the true length by 5% (1.41 and 1.55 m, respectively).

These findings are important because if a study is analyzing measurements that are from more than one drone, the uncertainty associated with those measurements must be taken into account to know if measurements are reliable and comparable. For instance, let’s say we are comparing the body length of two different populations and found that population A is significantly longer than population B. From looking at Figure 3, that significant difference in length between population A and B could be unreliable as the difference may be due to the bias introduced by the type of drone, camera sensor, focal length lens, and whether a barometer or laser altimeter was used for recording altitude. In other words, without incorporating uncertainty associated with each measurement, how do you trust your measurement? 

Hence, the National Institute of Standards and Technology (NIST) states that a measurement is complete only when accompanied by a quantitative statement of its uncertainty (Taylor & Kuyatt, 1994). In our Bierlich et al. (2021) study, we develop a Bayesian statistical model where we use the measurements of the known-sized object floating at the surface (what was used for Fig. 3) as training data to predict the lengths of unknown-sized whales. This Bayesian approach views data and the underlying parameters that generated the data (such as the mean or standard deviation) as random, and thus can be described by a statistical distribution. Using Bayes’ Theorem, a model of the observed data (called the likelihood function), is combined with prior knowledge pertaining to the underlying parameters (called the prior probability distribution) to form the posterior probability distribution, which serves as updated knowledge about the underlying parameter. For example, if someone told me they saw a 75 ft blue whale, I would not be phased. But if someone told me they saw a 150 ft blue whale, I would be skeptical – I’m using prior knowledge to determine the probability of this statement being true. 

The posterior probability distribution produced by this Bayesian approach can also serve as new prior information for subsequent analyses. Following this framework, we used the known-sized objects to first estimate the posterior probability distribution for error for each drone. We then used that posterior probability distribution for error specific to each drone platform as prior information to form a posterior predictive distribution for length of unknown-sized whales. The length of an individual whale can then be described by the mean of this second posterior predictive distribution, and its uncertainty defined as the variance or an interval around the mean (Fig. 4). 

Figure 4. An example of a posterior predictive distribution for total length of an individual blue whale. The black bars represent the uncertainty around the mean value (the black dot) – the longer black bars represent the 95% highest posterior density (HPD) interval, and the shorter black bars represent the 65% HPD interval. 

For over half a decade, the GEMM Lab has been collecting drone images of Pacific Coast Feeding Group (PCFG) of gray whales off the coast of Oregon to measure their morphology and body condition (see GRANITE Project Blog). We have been using several different types of drones equipped with different cameras, focal length lenses, barometers, and laser altimeters. These measurements from different drones will inherently have different levels of error associated with them, so adapting these methods for incorporating uncertainty will be key to ensure our measurements are comparable and analyses are robust. To do this, we fly over a known-sized board (1 m) at the start of each flight to use as training data to generate a posterior predictive distribution for length of the an unknown-sized PCFG gray whale that we fly over (Fig. 5). Likewise, we are working closely with several other collaborators who are also using different drones. Incorporating measurement uncertainty from drones used across research labs and in different environments will help ensure robust analyses and provide great opportunity for some interesting comparisons – such as differences in gray whale body condition on their feeding grounds in Oregon vs. their breeding grounds in Baja, Mexico, and morphological comparisons with other baleen whale species, such as blue and humpback whales. We are currently wrapping up measurement from thousands of boards (Fig. 5) and whales (Fig. 1) from 2016 – 2021, so stay tuned for the results!

Figure 5. An example of a known-sized object (1 m long board) used as training data to assess measurement uncertainty. 

References

Bierlich, K.C., Schick, R.S., Hewitt, J., Dale, J., Goldbogen, J.A., Friedlaender, A.S., Johnston D.J. (2021). A Bayesian approach for predicting photogrammetric uncertainty in morphometric measurements derived from UAS. Marine Ecology Progress Series. DOI: https://doi.org/10.3354/meps13814

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. Mar Ecol Prog Ser 592: 267−281

Dawson SM, Bowman MH, Leunissen E, Sirguey P (2017) Inexpensive aerial photogrammetry for studies of whales and large marine animals. Front Mar Sci 4: 366

Gough, W.T., Segre, P.S., Bierlich, K.C., Cade, D.E., Potvin, J., Fish, F. E., Dale, J., di Clemente, J., Friedlaender, A.S., Johnston, D.W., Kahane-Rapport, S.R., Kennedy, J., Long, J.H., Oudejans, M., Penry, G., Savoca, M.S., Simon, M., Videsen, S.K.A., Visser, F., Wiley, D.N., Goldbogen, J.A. (2019). Scaling of swimming performance in baleen whales. Journal of Experimental Biology222(20).https://doi.org/10.1242/jeb.204172  

Taylor, B. N., and Kuyatt, C. E. (1994). Guidelines for Evaluating and Expressing the Uncertainty of NIST Measurement Results. Washington, DC: National Institute of Standards and Technology. 1–25.

Torres, W.I., & Bierlich, K.C. (2020). MorphoMetriX: a photogrammetric measurement GUI for morphometric analysis of megafauna. Journal of Open Source Software5(45), 1825. https://doi.org/10.21105/joss.01825  

Wei S, Dan G, Chen H (2016) Altitude data fusion utilizing differential measurement and complementary filter. IET Sci Meas Technol (Singap) 10: 874−879

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.

Learning from teaching

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

Based on my undergrad experience I assumed that most teaching in grad school would be as a teaching assistant, and this would consist of teaching labs, grading, leading office hours, etc. However, now that I’m in graduate school, I realize that there are many different forms of teaching as a graduate student. This summer I worked as an instructor for an e-campus course, which mainly involved grading and mentoring students as they developed their own projects. Yet, this past week I was a guest teacher for Physiology and Behavior of Marine Megafauna, which was a bit more involved.

I taught a whale photogrammetry lab that I originally developed as a workshop with a friend and former lab mate, KC Bierlich, at the Duke University Marine Robotics and Remote Sensing (MaRRS) lab when I worked there. Similar to Leila’s work, we were using photogrammetry to measure whales and assess their body condition. Measuring a whale is a deceivingly simple task that gets complicated when taking into account all the sources of error that might affect measurement accuracy. It is important to understand the different sources of error so that we are sure that our results are due to actual differences between whales instead of differences in errors.

Error can come from distortion due to the camera lens, inaccurate altitude measurements from the altimeter, the whale being arched, or from the measurement process. When we draw a line on the image to make a measurement (Image 1), measurement process errors come from the line being drawn incorrectly. This potential human error can effect results, especially if the measurer is inexperienced or rushing. The quality of the image also has an effect here. If there is glare, wake, blow or refraction covering or distorting the measurer’s view of the full body of the whale then the measurer has to estimate where to begin and end the line. This estimation is subjective and, therefore, a source of error. We used the workshop as an opportunity to study these measurement process errors because we could provide a dataset including images of varying qualities and collect data from different measurers.

Image 1. Screenshot of measuring the widths along a minke whale in MorphoMetriX. Source: https://github.com/wingtorres/morphometrix/blob/master/images/Picture4.png

This workshop started as a one-day lecture and lab that we designed for the summer drone course at the Duke Marine Lab. The idea was to simultaneously teach the students about photogrammetry and the methods we use, while also using all the students’ measurements to study the effect of human error and image quality on measurement accuracy. Given this one-day format, we ambitiously decided to teach and measure in the morning, compile and analyze the students’ measurements over lunch, and then present the results of our error analysis in the afternoon. To accomplish this, we prepared as much as we could and set up all the code for the analysis ahead of time. This preparation meant several days of non-stop working, discussing, and testing, all to anticipate any issues that might come up on the day of the class.  We used the measuring software MorphoMetriX (Torres & Bierlich, 2020) that was developed by KC and a fellow Duke Marine Lab grad student Walter Torres. MorphoMetriX was brand new at the time, and this newness of the software meant that we didn’t yet know all the issues that might come up and we did not have time to troubleshoot. We knew this meant that helping the students install the software might be a bit tricky and sure enough, all I remember from the beginning of that first lab is running around the room helping multiple people troubleshoot at the same time, using use all the programming knowledge I had to discover new solutions on the fly.

While troubleshooting on the fly can be stressful and overwhelming, I’ve come to appreciate it as good practice. Not only did we learn how to develop and teach a workshop, we also used what we had learned from all the troubleshooting to improve the software. I also used the code we developed for the analysis as the starting blocks for a software package I then wrote, CollatriX (Bird & Bierlich, 2020), as a follow up software to MorphoMetriX. Aside from the initial troubleshooting stress, the workshop was a success, and we were excited to have a dataset to study measurement process errors. Given that we already had all the materials for the workshop prepared, we decided to run a few more workshops to collect more data.

That brings me to my time at here at OSU. I left the Duke MaRRS lab to start graduate school shortly after we taught the workshop. Interested in running the workshop here, I reached out to a few different people. I first ran the workshop here as an event organized by the undergraduate club Ocean11 (Image 2). It was fun running the workshop a second time, as I used what I learned from the first round; I felt more confident, and I knew what the common issues would likely be and how to solve them. Sure enough, while there were still some troubleshooting issues, the process was smoother and I enjoyed teaching, getting to know OSU undergraduate students, and collecting more data for the project.

Image 2. Ocean11 students measuring during the workshop (Feb 7, 2020).
Image credit: Clara Bird

The next opportunity to run the lab came through Renee Albertson’s physiology and behavior of marine megafauna class, but during the COVID era this class had other challenges. While it’s easier to teach in person, this workshop was well suited to be converted to a remote activity because it only requires a computer, the data can be easily sent to the students, and screen sharing is an effective way to demonstrate how to measure. So, this photogrammetry module was a good fit for the marine megafauna class this term that has been fully remote due to COVID-19.  My first challenge was converting the workshop into a lab assignment with learning outcomes and analysis questions. The process also involved writing R code for the students to use and writing step-by-step instructions in a way that was clear and easy to understand. While stressful, I appreciated the process of developing the lab and these accompanying materials because, as you’ve probably heard from a teacher, a good test of your understanding of a concept is being able to teach it. I was also challenged to think of the best way to communicate and explain these concepts. I tried to think of a few different explanations, so that if a student did not understand it one way, I could offer an alternative that might work better. Similar to the preparation for the first workshop, I also prepared for troubleshooting the students’ issues with the software. However, unlike my previous experiences, this time I had to troubleshoot remotely.

After teaching this photogrammetry lab last week my respect for teachers who are teaching remotely has only increased. Helping students without being able to sit next to them and walk them through things on their computer is not easy. Not only that, in addition to the few virtual office hours I hosted, I was primarily troubleshooting over email, using screen shots from the students to try and figure out what was going on. It felt like the ultimate test of my programming knowledge and experience, having to draw from memories of past errors and solutions, and thinking of alternative solutions if the first one didn’t work. It was also an exercise in communication because programming can be daunting to many students; so, I worked to be encouraging and clearly communicate the instructions. All in all, I ended this week feeling exhausted but accomplished, proud of the students, and grateful for the reminder of how much you learn when you teach.

References

Bird, C. N., & Bierlich, K. (2020). CollatriX: A GUI to collate MorphoMetriX outputs. Journal of Open Source Software, 5(51), 2328. https://doi.org/10.21105/joss.02328

Torres, W., & Bierlich, K. (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

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.