The teamwork of conservation science

Dr. Leigh Torres
PI, Geospatial Ecology of Marine Megafauna Lab, Marine Mammal Institute
Assistant Professor, Oregon Sea Grant, Department of Fisheries and Wildlife, Oregon State University

I have played on sports teams all my life – since I was four until present day. Mostly soccer teams, but a fair bit of Ultimate too. Teams are an interesting beast. They can be frustrating when communication breaks down, irritating when everyone is not on the same timeline, and disastrous if individuals do not complete their designated job. Yet, without the whole team we would never win. So, on top of the fun of competition, skill development, and exercise, playing on teams has always been part of the challenging and fulfilling process for me: everyone working toward the same goal – to win – by making the team fluid, complimentary, integrated, and ultimately successful.

I have come to learn that it is the same with conservation science.

A few of my teams through the ages, as player and coach. Some of my favorite people are on these teams, from 1981 to 2018.

Conservation efforts are often so complex, that it is practically impossible to achieve success alone. Forces driving the need for conservation typically include monetary needs/desires, social values, ecological processes, animal physiology, multi-jurisdictional policies, and human behavior. Each one of these forces alone is challenging to understand and takes expertise to comprehend the situation. Hence, building a well-functioning team is essential. Here’s a recent example from the GEMM Lab:

Since 2014 entanglements of blue, humpback and gray whales in fishing gear along the west coast of the USA have dramatically increased, particularly in Dungeness crab fishing gear. Many forces likely led to this increase, including increased whale population abundance, potential shifts in whale distributions, and changes in fishing fleet dynamics. While we cannot point a finger at one cause, many people and groups recognize that we cannot continue to let whales become entangled and killed at such high rates: whale populations would decline, fisheries would look bad in the public eye and potentially lose profits, whales have an intrinsic right to live in the ocean without being bycaught, and whales are an important part of the ecosystem that would deteriorate without them. In 2017, the Oregon Whale Entanglement Working Group was formed to bring stakeholders together that were concerned about this problem to discuss possible solutions and paths forward. I was lucky to be a part of this group, which also included members of the Dungeness crab fishery and commission, the Oregon Department of Fish and Wildlife (ODFW), other marine mammal scientists, and representatives of the American Cetacean Society, The Nature Conservancy, and a local marine gear supplier.

We met regularly over 2.5 years, and despite some hesitation at first about walking into a room of potentially disgruntled fishermen (I would be lying if I did not admit to this), after the first meeting I looked forward to every gathering. I learned an immense amount about the Dungeness crab fishery and how it operates, how ODFW manages the fishery and why, and what people do, don’t and need to know about whales in Oregon. Everyone agreed that reducing whale entanglements is needed, and a frequent approach discussed was to reduce risk by not setting gear where and when we expect whales to be. Yet, this idea flagged a very critical knowledge gap: We do not have a good understanding of whale distribution patterns in Oregon. Thus leading to the development of a highly collaborative research effort to describe whale distribution patterns in Oregon and identify areas of co-occurrence between whales and fishing effort to reduce the risk of entanglements. Sounds great, but a tough task to accomplish in a few short years. So, let me introduce the great team I am working with to make it all happen.

While I may know a few things about whales and spatial ecology, I don’t know too much about fisheries in Oregon. My collaboration with folks at ODFW, particularly Kelly Corbett and Troy Buell, has enabled this project to develop and go forward, and ultimately will lead to success. These partners provide feedback about how and where the fishery operates so I know where and when to collect data, and importantly they will provide the information on fishing effort in Oregon waters to relate to our generated maps of whale distribution. This spatial comparison will produce what is needed by managers and fishermen to make informed and effective decisions about where to fish, and not to fish, so that we reduce whale entanglement risk while still harvesting successfully to ensure the health and sustainability of our coastal economies.

So, how can we collect standardized data on whale distribution in Oregon waters without breaking the bank? I tossed this question around for a long time, and then I looked up to the sky and wondered what that US Coast Guard (USCG) helicopter was flying around for all the time. I reached out to the USCG to enquire, and proposed that we have an observer fly in the helicopter with them along a set trackline during their training flights. Turns out the USCG Sector North Bend and Columbia River were eager to work with us and support our research. They have turned out to be truly excellent partners in this work. We had some kinks to work out at the beginning – lots of acronyms, protocols, and logistics for both sides to figure out – but everyone has been supportive and pleasant to work with. The pilots and crew are interested in our work and it is a joy to hear their questions and see them learn about the marine ecosystem. And our knowledge of helicopter navigation and USCG duties has grown astronomically.

On the left is a plot of the four tracklines we survey for whales each month for two years aboard a US Coast Guard helicopter. On the right are some photos of us in action with our Coast Guard partners.

Despite significant cost savings to the project through our partnership with the USCG, we still need funds to support time, gear and more. And full credit to the Oregon Dungeness Crab Commission for recognizing the value and need for this project to support their industry, and stepping up to fund the first year of this project. Without their trust and support the project may not have got off the ground. With this support in our back pocket and proof of our capability, ODFW and I teamed up to approach the National Oceanographic and Atmospheric and Administration (NOAA) for funds to support the remaining years of the project. We found success through the NOAA Fisheries Endangered Species Act Section 6 Program, and we are now working toward providing the information needed to protect endangered and threatened whales in Oregon waters.

Despite our cost-effective and solid approach to data collection on whale occurrence, we cannot be everywhere all the time looking for whales. So we have also teamed up with Amanda Gladics at Oregon Sea Grant to help us with an important outreach and citizen science component of the project. With Amanda we have developed brochures and videos to inform mariners of all kinds about the project, objectives, and need for them to play a part. We are encouraging everyone to use the Whale Alert app to record their opportunistic sightings of whales in Oregon waters. These data will help us build and test our predictive models of whale distribution. Through this partnership we continue important conversations with fishermen from many fisheries about their concerns, where they are seeing whales, and what needs to be done to solve this complex conservation challenge.  

Of course I cannot collect, process, analyze, and interpret all this data on my own. I do not have the skills or capacity for that. My partner in the sky is Craig Hayslip, a Faculty Research Assistant in the Marine Mammal Institute. Craig has immense field experience collecting data on whales and is the primary observer on the survey flights. Together we have navigated the USCG world and developed methods to collect our data effectively and efficiently (all within a tiny space flying over the ocean). In a few months we will be ¾ of the way through our data collection phase, which means data analysis will take over. For this phase I am bringing back a GEMM Lab star, Solene Derville, who recently completed her PhD. As the post-doc on the project, Solene will take the lead on the species distribution modeling and fisheries overlap analysis. I am looking forward to partnering with Solene again to compile multiple data sources on whales and oceanography in Oregon to produce reliable and accurate predictions of whale occurrence and entanglement risk. Finally I want to acknowledge our great partners at the Cascadia Research Collective (Olympia, WA) and the Cetacean Conservation and Genomics Lab (OSU, Marine Mammal Institute) who help facilitate our data collection, and conduct the whale photo-identification or genetic analyses to determine population assignment.  

As you can see, even this one, smallish, conservation research project takes a diverse team of partners to proceed and ensure success. On this team, my position is sometimes a player, coach, or manager, but I am always grateful for these amazing collaborations and opportunities to learn. I am confident in our success and will report back on our accomplishments as we wrap up this important and exciting conservation science project.   

A fin whale observed off the Oregon coast during one of our surveys aboard a US Coast Guard helicopter.

What are the ecological impacts of gray whale benthic feeding?

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

Happy new year from the GEMM lab! Starting graduate school comes with a lot of learning. From skills, to learning about how much there is to learn, to learning about the system I will be studying in depth for the next few years. This last category has been the most exciting to me because digging into the literature on a system or a species always leads to the unearthing of some fascinating and surprising facts. So, for this blog I will write about one of the aspects of gray whale foraging that intrigues me most: benthic feeding and its impacts.

How do gray whales feed?

Gray whales are a unique species. Unlike other baleen whales, such as humpback and blue whales, gray whales regularly feed off the bottom of the ocean (Nerini, 1984). They roll to one side and swim along the bottom, they then suction up (by depressing their tongue) the sediment and prey, then the sediment and water is filtered out of the baleen. In fact, we use sediment streams, shown in Figure 1, as an indicator of benthic feeding behavior when analyzing drone footage (Torres et al. 2018).

Figure 1. Screenshot of drone video showing sediment streaming from mouth of a whale after benthic feeding. Video taken under NOAA/NMFS permit #21678

Locations of benthic feeding can be identified without directly observing a gray whale actively feeding because of the excavated pits that result from benthic feeding (Nerini 1984). These pits can be detected using side-scan sonar that is commonly used to map the seafloor. Oliver and Slattery (1985) found that the pits typically are from 2-20 m2. In some of the imagery, consecutive neighboring pits are visible, likely created by one whale in series during a feeding event. Figure 2 shows different arrangements of pits.

Figure 2. Different arrangements of pits created by feeding whales (Nerini 1984).

Aside from how fascinating the behavior is, benthic feeding is also interesting because it has a large impact on the environment. Coming from a background of studying baleen whales that primarily feed on krill, I had not really considered the potential impacts of whale foraging other than removing prey from the environment. However, when gray whales feed, they excavate large areas of the benthic substrate that disturb and impact the habitat.

The impacts of benthic feeding

Weitkamp et al. (1992) conducted a study on gray whale benthic foraging on ghost shrimp in Puget Sound, WA, USA. This study, conducted over two years, focused on measuring the impact of benthic foraging by its effect on prey abundance. They found that the standing stock of ghost shrimp within a recently excavated pit was two to five times less than that outside the pit, and that 3100 to 5700 grams of shrimp can be removed per pit. From aerial surveys they estimated that within one season feeding gray whales created between 2700 and 3200 pits. Using these values, they calculated that 55 to 79% of the standing stock of ghost shrimp was removed each season by foraging gray whales. Interestingly, they found that the shrimp biomass within an excavated pit recovered within about two months.

Oliver and Slattery (1985) also found a recovery period of about 2 months per pit in their study on the effect of gray whale benthic feeding on the prey community in the Bering Sea. They sampled prey within and outside feeding excavations, both actual whale pits and man-made, to test the response of the benthic community to the disturbance of a feeding event. They found that after the initial feeding disturbance, the excavated area was rapidly colonized by scavenging lysianassid amphipods, which are small (10 mm) crustaceans that typically eat dead organic material. These amphipods rushed in and attacked the organisms that were injured or dislodged by the whale feeding event, typically small crustaceans and polychaete worms. Within hours of the whale feeding event, these amphipods had dispersed and a different genre of scavenging lysianassid amphipods slowly invaded the excavated pit further and stayed much longer. After a few days or weeks these pits collected and trapped organic debris that attracted more colonists. Indeed, they found that the number of colonists remained elevated within the excavated areas for over two months.

Notably, these results on how the disturbance of gray whale benthic feeding changes sediment composition support the idea that this foraging behavior maintains the sand substrate and therefore helps to maintain balanced levels of benthic dwelling amphipods, their primary source of prey in this study area (Johnson and Nelson, 1984). Gray whales scour the sea floor when they feed and this process leads to the resuspension of lots of sediments and nutrients that would otherwise remain on the seafloor. Therefore, while this feeding may seem like a violent disturbance, it may in fact play a large role in benthic productivity (Johnson and Nelson, 1984; Oliver and Slattery, 1985).

These ecosystem impacts of gray whale benthic feeding I have described above demonstrate the various stages of invaders after a feeding disturbance, and the process of succession. Succession is the ecological process of how a community structure builds and grows. Primary succession is when the structure grows from truly nothing and secondary succession occurs after a disturbance, such as a fire. In secondary succession, there are typically pioneer species that first appear and then give way to other species and a more complex community eventually emerges. Succession is well documented in many terrestrial studies after disturbance events, and the processes of secondary succession is very important to community ecology and resilience.

Since gray whale benthic foraging does not impact an entire habitat all at once, the process is not perfectly comparable to secondary succession in terrestrial systems. Yet, when thinking about the smaller scale, another example of succession in the marine environment takes place at a whale fall. When a whale dies and sinks to the ocean floor, a small ecosystem emerges. Different organisms arrive at different stages to scavenge different parts of the carcass and a food web is created around it.

To me the impacts of gray whale benthic feeding are akin to both terrestrial disturbance events and whale falls. The excavation serves as a disturbance, and through secondary succession the habitat is refreshed via stages of different species colonization until the system eventually returns to the pre-disturbance levels. However, like a whale fall the feeding event leaves behind injured or displaced organisms that scavengers consume; in fact seabirds are known to take advantage of benthic invertebrates that are brought to the surface by a gray whale feeding event (Harrison, 1979). 

So much of our research is focused on questions about how the changing environment impacts our study species and not the other way around. This venture into the literature has provided me with an important reminder to think about flipping the question. I have enjoyed starting 2020 with a reminder of how cool gray whales are, and that while a disturbance can initially be thought of as negative, it may actually bring about important, and positive, change.

References

Nerini, Mary. 1984. “A Review of Gray Whale Feeding Ecology.” In The Gray Whale: Eschrichtius Robustus, 423–50. Elsevier Inc. https://doi.org/10.1016/B978-0-08-092372-7.50024-8.

Oliver, J. S., and P. N. Slattery. 1985. “Destruction and Opportunity on the Sea Floor: Effects of Gray Whale Feeding.” Ecology 66 (6): 1965–75. https://doi.org/10.2307/2937392.

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

Weitkamp, Laurie A, Robert C Wissmar, Charles A Simenstad, Kurt L Fresh, and Jay G Odell. 1992. “Gray Whale Foraging on Ghost Shrimp (Callianassa Californiensis) in Littoral Sand Flats of Puget Sound, USA.” Canadian Journal of Zoology 70 (11): 2275–80. https://doi.org/10.1139/z92-304.

Johnson, Kirk R., and C. Hans Nelson. 1984. “Side-Scan Sonar Assessment of Gray Whale Feeding in the Bering Sea.” Science 225 (4667): 1150–52.

Harrison, Craig S. 1979. “The Association of Marine Birds and Feeding Gray Whales.” The Condor 81 (1): 93. https://doi.org/10.2307/1367866.

GEMM Lab 2019: A Year in the Life

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

Another year has come and gone, and with the final days of 2019 upon us, it is fulfilling to look back and summarize all of the achievements in the GEMM Lab this year. So, snuggle up with your favorite holiday drink and enjoy our recap of 2019!

We wrapped up two intense but rewarding gray whale field seasons this summer. Our project investigating the health of Pacific Coast Feeding Group (PCFG) gray whales through fecal hormone and body condition sampling in the context of ocean noise went into its fourth year, while the Port Orford project where we track whales and prey at a very fine-scale celebrated its wood anniversary (five years!). The dedication and hard work of lots of people to help us collect our data meant that we were able to add a considerable amount of samples to our growing gray whale datasets. Our trusty red RHIB Ruby zipped around the Pacific and enabled us to collect 58 fecal samples, fly the drone 102 times, undertake 105 GoPro drops and record 141 gray whale sightings. Our Newport crew was a mix of full-time GEMMers (Leigh, Todd, Dawn, Leila, Clara, and myself) as well as part-time summer GEMMers (Ale, Sharon, and Cassy). Further south in Port Orford, my team of undergraduate and high school students and I had an interesting field season. We only encountered four different individuals (Buttons, Glacier, Smudge, and Primavera), however saw them repeatedly throughout the month of August, resulting in as many as 15 tracklines for one individual. Furthermore, we collected 249 GoPro drops and 248 zooplankton net samples.  

The GEMM Lab’s fieldwork was not just restricted to gray whales. After last year’s successes aboard the NOAA ship Bell M. Shimada, Alexa and Dawn both boarded the ship again this year as marine mammal observers for the May and September cruises, respectively. They spied humpback, blue, sperm, and fin whales, as well as many dolphins and seabirds, adding to the GEMM Lab’s growing database of megafauna distribution off the Oregon coast. 

After winning the prestigious L’Oréal-UNESCO For Women in Science fellowship and the inaugural Louis Herman Scholarship, GEMM Lab grad Solène Derville lead her first research cruise aboard the French R/V Alis. She and her team conducted line transect surveys and micronekton/oceanographic sampling over several seamounts to try to solve the mystery of why humpbacks hang out there. We are also very excited to announce that Solène will be returning to the GEMM Lab as a post-doc in 2020! She will be creating distribution models of whales off the coast of Oregon with the data collected by Leigh during helicopter flights with the US Coast Guard. The primary aim of this work is to identify potential whale hotspots in an effort to avoid spatial overlap with fisheries gear and reduce entanglement risk.

Switching the focus from marine mammals to seabirds, Rachael has had an extremely busy year of field work all across the globe. She island-hopped from Midway (Hawaiian Northwest island) to the Falkland Islands in the first half of the year, and is currently overwintering on South Georgia, where she will be until end of February. Rachael is tracking albatross at all three locations by tagging individual birds to understand movements relative to fishing vessels and flight energetics. 

Besides several field efforts, the GEMM Lab was also busy disseminating our research and findings to various audiences. Our conferences kicked off in late February when Leigh and Rachael both flew to Kauai to present at the Pacific Seabird Group’s 46th Annual Meeting. In the spring, Leila, Dawn, Alexa, Dom, and myself drove to Seattle where the University of Washington hosted the Northwest Student Society of Marine Mammalogy chapter meeting and we all gave talks. Additionally, the Fisheries & Wildlife grad students in the lab also presented at the department’s annual Research Advances in Fisheries, Wildlife, and Ecology conference. Later in the year, Dom and I attended the State of the Coast conference where Dom was invited to participate in a panel about the holistic approaches to management in the nearshore while I presented a poster on preliminary findings of my Master’s thesis. Most recently, the entire GEMM Lab (bar Rachael) flew to Barcelona to present at the World Marine Mammal Conference (WMMC). 

Our science communication and outreach efforts were not just restricted to conferences though. Over the course of this year, the GEMM Lab supervised a total of 10 undergraduate and high school interns that assisted in a variety of ways (field and/or lab work, data analyses, independent projects) on a number of projects going on in the lab. Leigh and Dawn boarded the R/V Oceanus in the fall to co-lead a STEM research cruise aimed at providing high school students and teachers hands-on marine research. Dawn and I were guests on Inspiration Dissemination, a live radio show run by graduate students about graduate research going on at OSU. Our weekly blog, now in its fifth year, reached its highest viewership with a total of 14,814 views this year!

The GEMMers were once again prolific writers too! The 13 new publications in 10 scientific journals include contributions from Leigh (7), Rachael (6), Solène (2), Dawn (2), and Leila (1). Scroll down to the end of the post to see the list.

Academic milestones were also reached by several of us. Most notably and recently, Dom successfully defended his Master’s thesis this past week – congratulations Dom!! Unsurprisingly, he already has a job lined up starting in January as a Science Officer with the California Ocean Science Trust. Dom is the 6th GEMM Lab graduate, which after just five years of the GEMM Lab existing is a huge testament to Leigh as an advisor. Leila, who is in the 4th year of her PhD, anticipates finishing this coming March. We also had three successful research reviews – I met with my committee in late March to discuss my Master’s proposal, while Alexa and Dawn met with their committees in the summer to review their PhD proposals. All three reviews were fruitful and successful. And we want to highlight the success of a GEMM Lab grad, Florence Sullivan, who started a job in Maui with the Pacific Whale Foundation in September as a Research Analyst.

Leigh was recognized for her expertise in gray whale ecology and was appointed to the IUCN Western Gray Whale Advisory Panel (WGWAP). The western gray whales are a critically endangered population. At one point in the 1960s, the population was so scarce that they were believed to have been extinct. While this concern did not prove to be the case, the population still is not doing well, which is why the IUCN formed WGWAP to provide advice on the conservation of the western gray whales. Leigh was appointed to the panel this year and traveled to Switzerland and Russia for meetings. 

Clara aboard Ruby on her first day of gray whale field work in Oregon. Photo: Leigh Torres

We are excited about a new addition to the lab. Clara Bird started her MS in Wildlife Science in the Department of Fisheries & Wildlife this fall. She jumped straight into field work when she came in early September and got a taste of the Pacific. Clara joins us from the Duke University where she did her undergraduate degree and worked for the past year in their Marine Robotics and Remote Sensing Lab. Clara is digging into the gray whale drone footage collected over the last four field seasons and scrutinize them from a behavioral point of view. 

If you are reading this post, we would like to say that we really appreciate your support and interest in our work! We hope you will continue to join us on our journeys in 2020. Until then, happy holidays from the GEMM Lab!  

GEMM Lab at the beginning of June with some permanents GEMMs and some temporary summer GEMM helpers.

Barlow, D. R., M. Fournet, and F. Sharpe. 2019. Incorporating tides into the acoustic ecology of humpback whales. Marine Mammal Science 35:234-251.

Barlow, D. R., A. L. Pepper, and L. G. Torres. 2019. Skin deep: an assessment of New Zealand blue whale skin condition. Frontiers in Marine Science doi.org/10.3389/fmars.2019.00757.

Baylis, A. M. M., R. A. Orben, A. A. Arkhipkin, J. Barton, R. L. Brownell Jr., I. J. Staniland, and P. Brickle. 2019. Re-evaluating the population size of South American fur seals and conservation implications. Aquatic Conservation: Marine and Freshwater Ecosystems 29(11):1988-1995.

Baylis, A. M. M., M. Tierney, R. A. Orben, et al. 2019. Important at-sea areas of colonial breeding marine predators on the southern Patagonian Shelf. Scientific Reports 9:8517. 

Cockerham, S., B. Lee, R. A. Orben, R. M. Suryan, L. G. Torres, P. Warzybok, R. Bradley, J. Jahncke, H. S. Young, C. Ouverney, and S. A. Shaffer. 2019. Microbial biology of the western gull (Larus occidentalis). Microbial Ecology 78:665-676.

Derville, S., L. G. Torres, R. Albertson, O. Andrews, C. S. Baker, P. Carzon, R. Constantine, M. Donoghue, C. Dutheil, A. Gannier, M. Oremus, M. M. Poole, J. Robbins, and C. Garrigue. 2019. Whales in warming water: assessing breeding habitat diversity and adaptability in Oceania’s changing climate. Global Change Biology 25(4):1466-1481.

Derville, S., L. G. Torres, R. Dodémont, V. Perard, and C. Garrigue. 2019. From land and sea, long-term data reveal persistent humpback whale (Megaptera novaeangliae) breeding habitat in New Caledonia. Aquatic Conservation: Marine and Freshwater Ecosystems 29(10):1697-1711.

Fleischman, A. B., R. A. Orben, N. Kokubun, A. Will, R. Paredes, J. T. Ackerman, A. Takahashi, A. S. Kitaysky, and S. A. Shaffer. 2019. Wintering in the western Subantarctic Pacific increases mercury contamination of red-legged kittiwakes. Environmental Science & Technology 53(22):13398-13407.

Holdman, A. K., J. H. Haxel, H. Klinck, and L. G. Torres. 2019. Acoustic monitoring reveals the times and tides of harbor porpoise (Phocoena phocoena) distribution off central Oregon, U.S.A. Marine Mammal Science 35:164-186.

Kroeger, C., D. E. Crocker, D. R. Thompson, L. G. Torres, P. Sagar, and S. A. Shaffer. 2019. Variation in corticosterone levels in two species of breeding albatrosses with divergent life histories: responses to body condition and drivers of foraging behavior. Physiological and Biochemical Zoology 92(2):223:238.

Loredo, S. A., R. A. Orben, R. M. Suryan, D. E. Lyons, J. Adams, and S. W. Stephensen. 2019. Spatial and temporal diving behavior of non-breeding common murres during two summers of contrasting ocean conditions. Journal of Experimental Biology and Ecology 517:13-24.

Monteiro, F., L. S. Lemos, J. Fulgêncio de Moura, R. C. C. Rocha, I. Moreira, A. P. Di Beneditto, H. A. Kehrig, I. C. A. C. Bordon, S. Siciliano, T. D. Saint’Pierre, and R. A. Hauser-Davis. 2019. Subcellular metal distributions and metallothionein associations in rough-toothed dolphins (Steno bredanensis) from southeastern Brazil. Marine Pollution Bulletin 146:263-273.

Orben, R. A., A. B. Fleischman, A. L. Borker, W. Bridgeland, A. J. Gladics, J. Porquez, P. Sanzenbacher, S. W. Stephensen, R. Swift, M. W. McKown, and R. M. Suryan. 2019. Comparing imaging, acoustics, and radar to monitor Leach’s storm-petrel colonies. PeerJ 7:e6721.

Yates, K. L., …, L. G. Torres, et al. 2019. Outstanding challenges in the transferability of ecological models. Trends in Ecology & Evolution 33(10):790-802.

Flying halfway around the world to learn about marine mammals from around the world!

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

The GEMM Lab is back from Barcelona after attending the World Marine Mammal Conference last week and it sure was a week to remember! Not only did every GEMM member present some aspect of their research at the conference (either as a poster, speed or full-length talk) but some of us also attended workshops, scheduled meetings with collaborators, new & old, and we certainly all learned a lot of new information about what is going on in marine mammalogy across the globe. Having had a few days now to reflect upon the intense four days spent at the conference, we want to highlight the talks that we each personally thought were some of the most interesting and exciting.

“Double Drone Drama” was the alliterative title of Héloïse Frouin-Mouy‘s talk about using two drones to collect simultaneous visual and underwater acoustic behavioral data of gray whales in Baja California, Mexico. While there were many talks during the week that discussed incorporating drones, also known as unmanned aerial vehicles (UAVs), into marine mammal research, this project was potentially the only one that discussed using two simultaneously. One drone collected visual aerial observations while the other obtained close-range passive acoustic measurements with an underwater recording hydrophone to better understand the behavioral contexts of call generation. Froiun-Mouy and her team detected call-type-specific source levels relative to behavior state through this dual-approach. For example, they were able to estimate the acoustic source levels of bubble-blasts produced by gray whales, and the double drone action recorded a variety of calls. Using two or more UAVs can provide a more integrated snapshot into the animal vocalization context, and it will be interesting to see whether this method is applied elsewhere on a variety of whale species.

Source: Twitter
Tara Sayuri Whitty. Source: UCSD Aquarium.

Tara Sayuri Whitty discussed her doctoral research focused on understanding the mental models of local, artisanal fishing communities at the heart of the vaquita conservation efforts. The vaquita has experienced rapid population declines due primarily to bycatch in gillnet fisheries from legal local gillnet fisheries and the illegal totoaba fishery. With the sole intent of preventing bycatch, gillnets were banned for legal practice, but the illegal totoaba fishery continued, as did vaquita bycatch. Whitty conducted interviews to understand the mental models and perceptions of local fishing communities towards officials and conservationists regarding the gillnet band. She discovered that these conservation efforts have not only failed to prevent vaquita bycatch, but they have now pitted conservationists against local communities because an important aspect of their livelihoods is now banned. This misstep and lack of trust with the community now threatens future conservation and recovery progress for the vaquita and highlights the need to collaborate and engage with local communities early and often when such efforts are so closely tied to human well-being.

Pauline Goulet. Source: Soundtags.

Pauline Goulet, a PhD student in the Sea Mammal Research Unit at the University of St. Andrews, presented findings obtained from a novel sonar tag deployed on southern elephant seals (SES) in the Kerguelen Islands and Peninsula Valdes. Gaining insight into predator-prey interactions is critical to understanding the ecology of marine mammals as they live in dynamic and vast environments where prey is patchy. Collecting in-situ prey information is difficult, and in some cases impossible, due to the remote locations where marine mammals forage and it is not being feasible to follow individuals around continuously to collect prey samples at every foraging event. In an attempt to overcome this universal challenge to marine mammal research, Goulet and her collaborators decided to mimic the experts in prey detection and visualization from a distance in the marine environment – echolocating odontocetes. By equipping conventional DTAGs with a 1.5 MHz single beam sonar with a 6 m detection range, Goulet was able to identify whether SES were pursuing individual fish or large schools of fish. Additionally, by also analyzing the accelerometer data, she could document whether prey capture attempts were successful or not, and link these results to the body condition of individual SES (inferred from the horizontal distance an individual traveled during drift dives, whereby a longer horizontal distance in the same period of time suggested that the individual had gained weight and was now heavier). It was ingenious to see researchers utilize a biological trait that evolved millions of years ago in certain marine mammal predators to better understand the ecology of another marine mammal predator.

A trio of talks given by Kristi Fazioli, Valeria Paz, and Shauna McBride-Kebert, in the ‘Habitat and Distribution II’ session, discussed responses of coastal bottlenose dolphins to hurricanes in the Gulf of Mexico (GoM). Besides continuing to be an area of interest in conservation after the Deepwater Horizon oil spill, the GoM frequently experiences hurricanes and other strong storm systems that cause extensive flooding events annually. Hence, dolphins along the GoM coast experience a large outflow of freshwater after severe precipitation, leading to low salinity events. Both Fazioli and Paz hypothesized that these changes in environmental conditions can create health problems to the dolphins.

Bottlenose dolphin underwater in the Gulf of Mexico. Source: Mike Heithaus.

Fazioli investigated encounter rates and skin conditions of bottlenose dolphins after Hurricane Harvey. She found that, in 2017, the encounter rates in her study area decreased, while skin lesions increased (Christina Toms, unpublished work, expected Spring 2020). Skin lesions are known to occur at higher rates after exposure to freshwater and even though they persist for some time, they eventually do heal. After less than two years, preliminary data suggest that these dolphins have returned to their original distributions in the study area. Paz’s study in Shark Bay Estuary examined different environmental drivers of dolphin distribution following Hurricane Irma. She found that dissolved oxygen, salinity, and temperature were the primary dynamic, environmental drivers of distribution following a major hurricane. Lastly, McBride’s species distribution models of bottlenose dolphins in response to severe flooding concluded that depth, slope, latitude, longitude, season, and dissolved oxygen all contributed in different percentages to distribution.

Marta Guerra. Source: RBR.

Marta Guerra presented findings from her PhD research at the University of Otago in New Zealand on the ecology and distribution of sperm whales in New Zealand. Kaikoura canyon is a region utilized by sperm whales for foraging, and Marta’s research highlighted marked differences in their distribution between the summer and winter, likely reflective of the sperm whales switching their target prey items seasonally. In the middle of their data collection period, a very intense earthquake struck the region in 2016, causing a canyon-flushing event that altered the canyon ecosystem. The sperm whales responded to this extreme event by altering their distribution away from the areas most affected by the earthquake, demonstrating that these marine predators respond to environmental shifts in the ecosystem they depend on at multiple scales. 

David Wiley. Source: NOAA.

On the final day of the conference, David Wiley gave a talk entitled “First documentation of coordinated bottom-feeding by humpback whales”. Using footage from tags containing a suite of sensors and video cameras, Wiley and colleagues observed humpback whales feeding on sand lace in the Stellwagen Bank National Marine Sanctuary. Sand lace are a species of fish that frequently burrow in the sand in an attempt to avoid capture by predators looking for their next meal. Humpback whales in the area have been observed with lacerations and scars along their mouths, originally leading to the hypothesis that whales were bottom-feeding. However, it was never known whether whales compete or cooperate when exploiting this resource and what the actual mechanics of this feeding behavior look like. The tag data revealed that groups of 3-4 individuals work together to approach the seafloor in a star-shape formation and when they get close enough, the sand lace emerge from the sand (probably an escape response to the approaching vibrations created by large whales) only to be engulfed by the humpbacks who are poised directly above them with wide-open mouths. Not only did the video footage reveal that individuals are so close together that their rostrums are almost touching, but Wiley and team were able to determine that whales perform their behavior usually within the same group of 3-4 individuals and that the orientation of each individual within the star-formation remains the same almost every time. This talk was so enjoyable because it was a reminder of how little we still know about marine mammals and provided a moment of audible awe and surprise throughout the room.

Barcelona-bound! The GEMM Lab heads to the World Marine Mammal Conference

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

Every two years, an international community of scientists, managers, policy-makers, educators, and students gather to share the most current research and most pressing conservation issues facing marine mammals. This year, the World Marine Mammal Conference will take place in Barcelona, Spain from December 7-12, and the whole GEMM Lab will make their way across the Atlantic to present their latest work. The meeting is an international gathering of scientists ranging from longtime researchers who have shaped the field throughout the course of their careers to students who are just beginning to carve out a niche of their own. This year’s conference has 2,500 registered attendees from 95 different countries, 1,960 abstract submissions, and 700 accepted oral and speed talks and 1,200 posters. Needless to say, it is an incredible platform for learning, networking, and putting our work in the context of research taking place around the globe.

This will be my third time at this conference. I attended in San Francisco in 2015 as a wide-eyed undergraduate and met with Leigh, who I hoped would soon become my graduate advisor. I also presented my Masters research at the conference in Halifax in 2017. This time around, I will be presenting findings from the first two chapters of my PhD. Looking ahead to the Barcelona 2019 meeting and having some sense of what to expect, I feel butterflies rising in my stomach—a perfect mixture of the nerves that come with putting your hard work out in the world, eagerness to learn and absorb new information, and excitement to reconnect with friends and colleagues from around the world. In short, I can’t wait!

For those of you reading this blog that are unable to attend, I’d like to share an overview of what the GEMM Lab will be presenting at the conference. If you will be in Barcelona, we warmly invite you to the following posters, speed talks, and oral presentations! In order of appearance:

Lisa Hildebrand, MS Student

What do Oregon gray whales like to eat? Do individual whales have individual foraging habits? To learn more visit Lisa Hildebrand’s poster “Investigating potential gray whale individual foraging specializations within the Pacific Coast Feeding Group”. (Poster presentation, Session: Foraging Ecology – Group A, Time: Monday, 1:30-3:00pm)

Todd Chandler, Faculty Research Assistant

Did you know it is possible to measure the mechanics of how a blue whale feeds using a drone? The GEMM Lab’s all-star drone pilot Todd Chandler will present a poster titled “More than snacks: An analysis of drone observed blue whale surface lunge feeding linked with prey data”. (Poster presentation, Session: Foraging Ecology – Group A, Time: Monday, 1:30-3:00pm)

Clara Bird, MS Student

The GEMM Lab’s newest student Clara Bird will present a poster on work she conducted with the Marine Robotics and Remote Sensing lab at Duke University using new technologies and approaches to investigate scarring patterns on humpbacks. Her poster is titled “A comparison of percent dorsal scar cover between populations of humpback whales (Megaptera novaeangliae) off California and the Western Antarctic Peninsula”. (Poster presentation, Session: New Technology  – Group B, Time: Tuesday, 8:30-9:45am)

Dr. Leigh Torres, Principal Investigator

GEMM Lab PI Leigh Torres will synthesize some exciting new analyses from the GEMM Lab’s gray whale physiology and ecology research off the Oregon Coast. Is it stressful to feed in a noisy coastal environment? Leigh will discuss the latest findings in her talk, “Sounds of stress: Evaluating the relationships between variable soundscapes and gray whale stress hormones”. (Oral presentation, Session: Physiology, Time: Tuesday, 11:30-11:45am)

Leila Lemos, PhD Student

Carrying on with exciting new findings about Oregon gray whales, Leila Lemos will present a speed talk titled “Stressed and slim or relaxed and chubby? A simultaneous assessment of gray whale body condition and hormone variability”, in which she will summarize three years of analysis of how gray whale health can be quantified, and how physiology is influenced by ocean conditions. (Speed talk, Session: Physiology, Time: Tuesday, 11:55am-12:m)

Dawn Barlow, PhD Student

Can we predict where blue whales will be using our understanding of their environment and prey? Can this knowledge be used for effective conservation? I (Dawn Barlow) will give a presentation titled “Cloudy with a chance of whales: Forecasting blue whale occurrence based on tiered, bottom-up models to mitigate industrial impacts”, which will share our latest findings on how functional ecological relationships can be modeled in changing ocean conditions. (Oral presentation, Session: Habitat and Distribution I, Time: Wednesday, 10:15-10:30am)

Dr. Solene Derville, Post-Doctoral Scholar

The GEMM Lab’s most recent graduate Solene Derville will present work she has conducted in New Caledonia regarding humpback whale diving and movement patterns around breeding grounds. Her speed talk is titled “Whales of the deep: Horizontal and vertical movements shed light on humpback whale use of critical pelagic habitats in the western South Pacific” (Speed talk, Session: Behavioral Ecology II, Time: Wednesday, 11:35-11:40am)

Dominique Kone, MS Student

Can sea otters make a comeback in Oregon after a long absence? Dom Kone takes a comprehensive look at how Oregon coast habitat could support a reintroduced sea otter population in his speed talk, “An evaluation of the ecological needs and effects of a potential sea otter reintroduction to Oregon, USA”. (Speed talk, Session: Conservation II, Time: Wednesday, 2:45-2:50pm)

Alexa Kownacki, PhD Student

Alexa Kownacki will share her latest findings on dolphin distribution relative to static and dynamic oceanographic variables in her speed talk titled “The biogeography of common bottlenose dolphins (T. truncatus) of the southwestern USA and Mexico”. (Speed talk, Session: Habitat and Distribution II, Time: Wednesday, 3:35-3:40pm)

Other members of the Marine Mammal Mnstitute who will present their work include: Scott Baker, Debbie Steel, Angie Sremba, Karen Lohman, Daniel Palacios, Bruce Mate, Ladd Irvine, and Robert Pitman. For anyone planning to attend, we look forward to seeing you there! For those who wish to stay tuned from home, keep your eye on the GEMM Lab twitter page for our updates during the conference and follow the conference hashtag #WMMC19, and look forward to future blog posts recapping the experience.

Measuring dolphin response to Navy sonar

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

During the summer of 2017 I was an intern for Cascadia Research Collective (CRC), a non-profit organization based out of Olympia, Washington, that conducts research on marine mammal behavior, ecology, and population status along the western US coast and around Hawaii. My internship was primarily office-based and involved processing photographs of humpback and blue whales along the US west coast to add to CRC’s long-term photo-identification catalogues. However, I was asked to join a research project investigating the behavioral and physiological responses of four dolphin species in southern California (Fig. 1). The research project is a collaborative effort lead by Dr. Brandon Southall and involves researchers from CRC, Kelp Marine Research, NOAA’s Southwest Fisheries Science Center, and SR3. Since my internship with CRC, there have been three pilot efforts and one full field effort of this project, called the SOCAL Tagless Behavioral and Physiological Response Study (BPRS), and I have been a part of all of them.

The marine environment is stressed out, and so are the millions of flora and fauna that inhabit the global ocean. Humans are a big contributor to this stress. During the last few decades, we have produced more and more things that have ended up in the ocean, whether by choice or by chance. Plastic pollution has become a pervasive and persistent problem, especially after the discovery that when large plastic items are exposed to UV light and seawater they break down into smaller pieces, termed micro- and nano-plastics (Jambeck et al. 2015). Increased demand for oil and gas to supply a growing human population has led to much more marine oil and gas exploration and exploitation (World Ocean Review 2013). Since 1985, global container shipping has increased by approximately 10% annually (World Ocean Review 2010) and it is estimated that global freight demand will triple by 2050 (International Transport Forum 2019). The list of impacts is long. Our impact on the earth, of which the ocean makes up 71%, has been so extreme that expert groups suggest that a new geological epoch – the Anthropocene – needs to be declared to define the time that we now find ourselves in and the impact humanity is having on the environment (Lewis and Maslin 2015). While this term has not been officially recognized, it is irrefutable that humans have and continue to alter ecosystems, impacting the organisms within them. 

Noise is an impact often overlooked when thinking about anthropogenic effects in the marine environment, likely because we as humans do not hear much of what happens beneath the ocean surface. However, ocean noise is of particular concern for cetaceans as sound is their primary sense, both over long and short distances. Sound travels extremely efficiently underwater and therefore anthropogenic sounds can be propagated for thousands of kilometers or more (Weilgart 2007a). While it is widely agreed upon that anthropogenic noise is likely a significant stressor to cetaceans (Weilgart 2007b; Wright et al. 2007; Tyack 2008), very few studies have quantified their responses to noise to date. This knowledge gap is likely because behavioral and physiological responses to sound can be subtle, short-lived or slowly proliferate over time, hence making them hard to study. However, growing concern over this issue has resulted in more research into impacts of noise on marine mammals, including the GEMM Lab’s impacts of ocean noise on gray whales project.

The most extreme impact of sound exposure on marine mammals is death. Mass strandings of a few cetacean species have coincided in time and space with Navy sonar operations (Jepson et al. 2003; Fernández et al. 2005; Filadelfo et al. 2009). While fatal mass strandings of cetaceans are extremely troubling, they are a relatively rare occurrence. A cause for perhaps greater concern are sub-lethal changes in important behaviors such as feeding, social interactions, and avoidance of key habitat as a result of exposure to Navy sonar. All of these potential outcomes have raised interest within the U.S. Navy to better understand the responses of cetaceans to sonar. 

The SOCAL Tagless BPRS is just one of several studies that has been funded by the U.S. Office of Naval Research to improve our understanding of Navy sonar impact on cetaceans, in particular the sub-lethal effects described earlier. It builds upon knowledge and expertise gained from previous behavioral response studies led by Dr. Southall on a variety of marine mammal species, including beaked whales, baleen whales, and sperm whales. Those efforts included deploying tags on individual whales to obtain high-resolution movement and passive acoustic data paired with controlled exposure experiments (CEEs) during which simulated Navy mid-frequency active sonar (MFAS) or real Navy sonar were employed. Results from that multi-year effort have shown that for blue whales, responses generally only lasted for as long as the sound was active and highly dependent on exposure context such as behavioral state, prey availability and the horizontal distance between the sound source and the individual whale. Blue whales identified as feeding in shallow depths showed no changes in behavior, however over 50% of deep-feeding whales responded during CEEs (Southall et al. 2019).

The SOCAL Tagless BPRS, as the name implies, does not involve deploying tags on the animals. Tags were omitted from this study design because tags on dolphins have not had high success rates of staying on for a very long time. Furthermore, dolphins are social species that typically occur in groups and individuals within a group are likely to interact or react together when exposed to an external stimuli. Therefore, the project integrates established methods of quantifying dolphin behavior and physiology in a novel way to measure broad and fine-scale group and individual changes of dolphin behavior and physiology to simulated Navy MFAS or real Navy sonars using CEEs. 

During these tagless CEEs, a dolphin group is tracked from multiple platforms using several different tools. Kelp Marine Research is our on-shore team that spots workable groups (workable meaning that a group should be within range of all platforms and not moving too quickly so that they will leave this range during the CEE), tracks the group using a theodolite (just like I do for my Port Orford gray whale project), and does focal follows to record behavior of the group over a period of time. Ziphiid, one of CRC’s RHIBs, is tasked with deploying three passive acoustic sensors to record sounds emitted by the dolphins and to measure the intensity of the sound of the simulated Navy MFAS or the real Navy sonars. Musculus, the second CRC RHIB, has a dual-function during CEEs; it holds the custom vertical line array sound source, which emits the simulated Navy MFAS, and it is also the ‘biopsy boat’ tasked with obtaining biopsy samples of individuals within the dolphin group to measure potential changes in stress hormone levels. And last but not least, the Magician, the third vessel on the water, serves as ‘home-base’ for the project (Fig. 3). Quite literally it is where the research team eats and sleeps, but it is also the spotting vessel from which visual observations occur, and it is the launch pad for the unmanned aerial system (UAS) used to measure potential changes in group composure, spacing, and speed of travel.

The project involves a lot of moving parts and we are careful to conduct the research with explicit monitoring and mitigation requirements to ensure our work is carried out safely and ethically. These factors, as well as the fact that we are working with live, wild animals that we cannot ‘control’, are why three pilot efforts were necessary. Our first ‘official’ phase this past October was a success: in just eight days we conducted 11 CEEs. Six of these involved experimental sonar transmissions (two being from real Navy sonars dipped from hovering helicopters) and five were no-sonar controls that are critical to be able to experimentally associate sonar exposure with potential response. There are more phases to come in 2020 and 2021 and I look forward to continue working on such a collaborative project.

For more information on the project, you can visit Southall Environmental Associates project page, or read the blog posts written by Dr. Brandon Southall (this one or this one).

For anyone attending the World Marine Mammal Conference in Barcelona, Spain, there will be several talks related to this research:

  • Dr. Brandon Southall will be presenting on the Atlantic BRS on beaked whales and short-finned pilot whales on Wednesday, December 11 from 2:15 – 2:30 pm
  • Dr. Caroline Casey will be presenting on the experimental design and results of this SOCAL Tagless BPRS project on Wednesday, December 11 from 2:30 – 2:45 pm

All research is authorized under NMFS permits #16111, 19091, and 19116 as well as numerous Institutional Animal Care and Use Committee and other federal, state, and local authorizations. More information is available upon request from the project chief scientist at Brandon.Southall@sea-inc.net

Literature cited

Fernández, A., J. F. Edwards, F. Rodríguez, A. Espinosa de los Monteros, P. Herráez, P. Castro, J. R. Jaber, V. Martín, and M. Arbelo. 2005. “Gas and fat embolic syndrome” involving a mass stranding of beaked whales (Family Ziphiidae) exposed to anthropogenic sonar signals. Veterinary Pathology 42(4):446-457.

Filadelfo, R., J. Mintz, E. Michlovich, A. D’Amico, P. L. Tyack, and D. R. Ketten. 2009. Correlating military sonar use with beaked whale mass strandings: what do the historical data show? Aquatic Mammals 35(4):435-444.

International Transport Forum. 2019. Transport demand set to triple, but sector faces potential disruptions. Retrieved from: https://www.itf-oecd.org/transport-demand-set-triple-sector-faces-potential-disruptions

Jambeck, J. R., R. Geyer, C. Wilcox, T. R. Siegler, M. Perryman, A. Andrady, R. Narayan, and K. L. Law. 2015. Plastic waste inputs from land into the ocean. Science 347(6223):768-771.

Jepson, P. D., M. Arbelo, R. Deaville, I A. P. Patterson, P. Castro, J. R. Baker, E. Degollada, H. M. Ross, P. Herráez, A. M. Pocknell, F. Rodríguez, F. E. Howie II, A. Espinosa, R. J. Reid, J. R. Jaber, V. Martin, A. A. Cunningham, and A. Fernández. 2003. Gas-bubble lesions in stranded cetaceans. Nature 425:575.

Lewis, S. L., and M. A. Maslin. 2015. Defining the Anthropocene. Nature 519:171-180.

Southall, B. L., S. L. DeRuiter, A. Friedlaender, A. K. Stimpert, J. A. Goldbogen, E. Hazen, C. Casey, S. Fregosi, D. E. Cade, A. N. Allen, C. M. Harris, G. Schorr, D. Moretti, S. Guan, and J. Calambokidis. 2019. Behavioral responses of individual blue whales (Balaenoptera musculus) to mid-frequency military sonar. Journal of Experimental Biology 222: doi. 10.1242/jeb.190637.

Tyack, P. L. 2008. Implications for marine mammals of large-scale changes in the marine acoustic environment. Journal of Mammalogy 89(3):549-558.

Weilgart, L. S. 2007a. The impacts of anthropogenic ocean noise on cetaceans and implications for management. Canadian Journal of Zoology 85(11):1091-1116.

Weilgart, L. S. 2007b. A brief review of known effects of noise on marine mammals. International Journal of Comparative Psychology 20(2):159-168.

World Ocean Review. 2014. WOR 3: Marine resources – opportunities and risks. Report No 3. Retrieved from: https://worldoceanreview.com/en/wor-3/oil-and-gas/.

World Ocean Review. 2010. WOR 1: Marine resources – Living with the oceans. A report on the state of the world’s oceans. Report No 1. Retrieved from: https://worldoceanreview.com/en/wor-1/transport/global-shipping/3/

Wright, A. J., N. A. Soto, A. L. Baldwin, M. Bateson, C. M. Beale, C. Clark, T. Deak, E. F. Edwards, A. Fernández, A. Godinho, L. T. Hatch, A. Kakuschke, D. Lusseau, D. Martineau, M. L. Romero, L. S. Weilgart, B. A. Wintle, G. Notarbartolo-di-Sciara, and V. Martin. Do marine mammals experience stress related to anthropogenic noise? International Journal of Comparative Psychology 20(2):274-316.

Classifying cetacean behavior

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

The GEMM lab recently completed its fourth field season studying gray whales along the Oregon coast. The 2019 field season was an especially exciting one, we collected rare footage of several interesting gray whale behaviors including GoPro footage of a gray whale feeding on the seafloor, drone footage of a gray whale breaching, and drone footage of surface feeding (check out our recently released highlight video here). For my master’s thesis, I’ll use the drone footage to analyze gray whale behavior and how it varies across space, time, and individual. But before I ask how behavior is related to other variables, I need to understand how to best classify the behaviors.

How do we collect data on behavior?

One of the most important tools in behavioral ecology is an ‘ethogram’. An ethogram is a list of defined behaviors that the researcher expects to see based on prior knowledge. It is important because it provides a standardized list of behaviors so the data can be properly analyzed. For example, without an ethogram, someone observing human behavior could say that their subject was walking on one occasion, but then say strolling on a different occasion when they actually meant walking. It is important to pre-determine how behaviors will be recorded so that data classification is consistent throughout the study. Table 1 provides a sample from the ethogram I use to analyze gray whale behavior. The specificity of the behaviors depends on how the data is collected.

Table 1. Sample from gray whale ethogram. Based on ethogram from Torres et al. (2018).

In marine mammal ecology, it is challenging to define specific behaviors because from the traditional viewpoint of a boat, we can only see what the individuals are doing at the surface. The most common method of collecting behavioral data is called a ‘focal follow’. In focal follows an individual, or group, is followed for a set period of time and its behavioral state is recorded at set intervals.  For example, a researcher might decide to follow an animal for an hour and record its behavioral state at each minute (Mann 1999). In some studies, they also recorded the location of the whale at each time point. When we use drones our methods are a little different; we collect behavioral data in the form of continuous 15-minute videos of the whale. While we collect data for a shorter amount of time than a typical focal follow, we can analyze the whole video and record what the whale was doing at each second with the added benefit of being able to review the video to ensure accuracy. Additionally, from the drone’s perspective, we can see what the whales are doing below the surface, which can dramatically improve our ability to identify and describe behaviors (Torres et al. 2018).

Categorizing Behaviors

In our ethogram, the behaviors are already categorized into primary states. Primary states are the broadest behavioral states, and in my study, they are foraging, traveling, socializing, and resting. We categorize the specific behaviors we observe in the drone videos into these categories because they are associated with the function of a behavior. While our categorization is based on prior knowledge and critical evaluation, this process can still be somewhat subjective.  Quantitative methods provide an objective interpretation of the behaviors that can confirm our broad categorization and provide insight into relationships between categories.  These methods include path characterization, cluster analysis, and sequence analysis.

Path characterization classifies behaviors using characteristics of their track line, this method is similar to the RST method that fellow GEMM lab graduate student Lisa Hildebrand described in a recent blog. Mayo and Marx (1990) analyzed the paths of surface foraging North Atlantic Right Whales and were able to classify the paths into primary states; they found that the path of a traveling whale was more linear and then paths of foraging or socializing whales that were more convoluted (Fig 1). I plan to analyze the drone GPS track line as a proxy for the whale’s track line to help distinguish between traveling and foraging in the cases where the 15-minute snapshot does not provide enough context.

Figure 1. Figure from Mayo and Marx (1990) showing different track lines symbolized by behavior category.

Cluster analysis looks for natural groupings in behavior. For example, Hastie et al. (2004) used cluster analysis to find that there were four natural groupings of bottlenose dolphin surface behaviors (Fig. 2). I am considering using this method to see if there are natural groupings of behaviors within the foraging primary state that might relate to different prey types or habitat. This process is analogous to breaking human foraging down into sub-categories like fishing or farming by looking for different foraging behaviors that typically occur together.

Figure 2. Figure from Hastie et al. (2004) showing the results of a hierarchical cluster analysis.

Lastly, sequence analysis also looks for groupings of behaviors but, unlike cluster analysis, it also uses the order in which behaviors occur. Slooten (1994) used this method to classify Hector’s dolphin surface behaviors and found that there were five classes of behaviors and certain behaviors connected the different categories (Fig. 3). This method is interesting because if there are certain behaviors that are consistently in the same order then that indicates that the order of events is important. What function does a specific sequence of behaviors provide that the behaviors out of that order do not?

Figure 3. Figure from Slooten (1994) showing the results of sequence analysis.

Think about harvesting fruits and vegetables from a garden: the order of how things are done matters and you might use different methods to harvest different kinds of produce. Without knowing what food was being harvested, these methods could detect that there were different harvesting methods for different fruits or veggies. By then studying when and where the different methods were used and by whom, we could gain insight into the different functions and patterns associated with the different behaviors. We might be able to detect that some methods were always used in certain habitat types or that different methods were consistently used at different times of the year.

Behavior classification methods such as these described provide a more refined and detailed analysis of categories that can then be used to identify patterns of gray whale behaviors. While our ultimate goal is to understand how gray whales will be affected by a changing environment, a comprehensive understanding of their current behavior serves as a baseline for that future study.

References

Burnett, J. D., Lemos, L., Barlow, D., Wing, M. G., Chandler, T., & Torres, L. G. (2019). Estimating morphometric attributes of baleen whales with photogrammetry from small UASs: A case study with blue and gray whales. Marine Mammal Science, 35(1), 108–139. https://doi.org/10.1111/mms.12527

Darling, J. D., Keogh, K. E., & Steeves, T. E. (1998). Gray whale (Eschrichtius robustus) habitat utilization and prey species off Vancouver Island, B.C. Marine Mammal Science, 14(4), 692–720. https://doi.org/10.1111/j.1748-7692.1998.tb00757.x

Hastie, G. D., Wilson, B., Wilson, L. J., Parsons, K. M., & Thompson, P. M. (2004). Functional mechanisms underlying cetacean distribution patterns: Hotspots for bottlenose dolphins are linked to foraging. Marine Biology, 144(2), 397–403. https://doi.org/10.1007/s00227-003-1195-4

Mann, J. (1999). Behavioral sampling methods for cetaceans: A review and critique. Marine Mammal Science, 15(1), 102–122. https://doi.org/10.1111/j.1748-7692.1999.tb00784.x

Slooten, E. (1994). Behavior of Hector’s Dolphin: Classifying Behavior by Sequence Analysis. Journal of Mammalogy, 75(4), 956–964. https://doi.org/10.2307/1382477

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

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

Detecting blue whales from acoustic data

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

In January of 2016, five underwater recording units were dropped to the seafloor in New Zealand to listen for blue whales (Fig. 1). These hydrophones sat listening for two years, brought to the surface only briefly every six months to swap out batteries and offload the data. Through all seasons and conditions when scientists couldn’t be on the water, they recorded the soundscape, generating a wealth of acoustic data with the potential to greatly expand our knowledge of blue whale ecology

Figure 1. Locations of the five Marine Autonomous Recording Units (MARUs) in the South Taranaki Bight region of New Zealand.

We have established that blue whales are present in New Zealand waters year-round 1. However, many questions remain regarding their distribution across daily, seasonal, and yearly scales. Our two-year acoustic dataset from five hydrophones throughout the STB region is a goldmine of information on blue whale occurrence patterns and the soundscape they inhabit. Having year-round occurrence data will allow us to examine what environmental and anthropogenic factors may influence blue whale distribution patterns. The hydrophones were listening for whales around the clock, every day, while we were on the other side of the world awaiting the recovery of the data to answer our questions.

Before any questions of seasonal distribution or anthropogenic impacts and noise can be addressed, however, we need to know something far more basic: when and where did we record blue whale vocalizations? This may seem like a simple, stepping-stone question, but it is actually quite involved, and the reason I spent the last month working with a team of acousticians at Cornell University’s Center for Conservation Bioacoustics. The expert research group here at Cornell, led by Dr. Holger Klinck, have been instrumental in our New Zealand blue whale research, including developing and building the recording units, hydrophone deployment and recovery, data processing, analysis, and advice. I am thrilled to work with all of them, and had an incredibly productive month of learning about acoustics from the best.

Blue whales produce multiple vocalizations that we are interested in documenting. The New Zealand song (Fig. 2A) is highly stereotyped and unique to the Southwest Pacific Ocean 2,3. Low-frequency downsweeps, or “D calls” (Fig. 2B), are far more variable and produced by blue whale populations around the world 4. Furthermore, Antarctic blue whales produce a highly-stereotyped “Z call” (Fig. 2C) and are known to be present in New Zealand waters occasionally 5.

Figure 2. Spectrograms of (A) the New Zealand blue whale song, (B), D calls, and (C) Antarctic Z calls.

One way to determine when blue whales were vocalizing is for an analyst to manually review the entirety of the two years of sound recordings for each of the five hydrophones by hand to scan for and select individual vocalizations. An alternative approach is to develop a detector algorithm to locate calls in the data based on their stereotypical characteristics. Over the past month I built, tested, and ran detectors for each blue whale call type using what is called a data template detector. This technique uses example signals from the data that the analyst selects as templates. The templates should be clear signals, and representative of the variation in calls contained in the dataset. Then, by comparing pixel characteristics between the template spectrograms and the spectrogram of the recording of interest using certain matching criteria (e.g. threshold for spectrogram correlation, detection frequency range), the algorithm searches for other signals like the templates in the full dataset. For example, in Fig. 3 you can see units of blue whale song I selected as templates for my detector.

Figure 3. Spectrogram of selected sound clips of New Zealand blue whale song, with units used as templates for a detector shown inside the teal boxes.

Testing the performance of a detector algorithm is critical. Therefore, a dataset is needed where calls were identified by an analyst and then used as the “ground truth”, to which the detector results are compared. For my ground truth dataset, I took a subset of 52 days and hand-browsed the spectrograms to identify and log New Zealand blue whale song, D calls, and Antarctic Z calls. In evaluating detector performance, there are three important metrics that need to be weighed: precision (the proportion of detections that are true), recall (the proportion of true calls identified by the detector), and false alarm rate (the number of false positive detections per hour). Ideally, the detector should be optimized to maximize precision and recall and minimize the false positives.

The STB region is highly industrial, and our two-year acoustic dataset contains periods of pervasive seismic airgun noise from oil and gas exploration. Ideally, a detector would be able to identify blue whale vocalizations even in the presence of airgun operations that dominate the soundscape for months. For blue whale song, the detector did quite well! With a precision of 0.91 and recall of 0.93, the detector could pick out song units over airgun noise (Fig. 4). A false alarm rate of 8 false positives per hour is a sacrifice worth making to identify song during seismic operations (and the false positives will be removed in a subsequent step). For D calls, seismic survey activity presented a different challenge. While the detector did well at identifying D calls during airgun operation, the first several detector attempts also logged every single airgun blast as a blue whale vocalization—clearly problematic. Through an iterative process of selecting template signals, and adjusting the number of templates used and the correlation threshold, I was able to come up with a detector which selected D calls and missed most airgun blasts. This success felt like a victory.

Figure 4. An example of spectrograms of simultaneous recordings from the five hydrophones illustrating seismic airgun noise (strong broadband signals that appear as repetitive black, vertical lines) overlapping New Zealand blue whale song. The red boxes are detection events selected by the detector, demonstrating its ability to capture song even during airgun operation.

After this detector development and validation process, I ran each detector on the full two-year acoustic dataset for all five recording units. This step was a good exercise in patience as I eagerly awaited the outputs for the many hours they took to run. The next step in the process will be for me to go through and validate each detector event to eliminate any false positives. However, running the detectors on the full dataset has allowed for exciting preliminary examinations of seasonal blue whale acoustic patterns, which need to be refined and expanded upon as the analysis continues. For example, sometimes the New Zealand song dominates the recordings on all hydrophones (Fig. 5), whereas other times of year song is less common. Similarly, there appear to be seasonal patterns in D calls and Antarctic Z calls, with peaks and dips in detections during different times of year.

Figure 5. An example spectrogram of simultaneous recordings from all five hydrophones during a time when New Zealand blue whale song dominated the recordings, with numerous, overlapping calls.

As with many things, the more questions you ask, the more questions you come up with. From preliminary explorations of the acoustic data my head is buzzing with ideas for further analysis and with new questions I hadn’t thought to ask of the data before. My curiosity has been fueled by scrolling through spectrograms, looking, and listening, and I am as excited as ever to continue researching blue whale ecology. I would like to thank the team at the Center for Conservation Bioacoustics for their support and guidance over the past month, and I look forward to digging deeper into the stories being told in the acoustic data!

Figure 6. A pair of blue whales observed in February 2017 in the South Taranaki Bight. Photo: L. Torres.

References

1.          Barlow, D. R. et al. Documentation of a New Zealand blue whale population based on multiple lines of evidence. Endanger. Species Res. 36, 27–40 (2018).

2.          McDonald, M. A., Mesnick, S. L. & Hildebrand, J. A. Biogeographic characterisation of blue whale song worldwide: using song to identify populations. J. Cetacean Res. Manag. 8, 55–65 (2006).

3.          Balcazar, N. E. et al. Calls reveal population structure of blue whales across the Southeast Indian Ocean and the Southwest Pacific Ocean. J. Mammal. 96, 1184–1193 (2015).

4.          Oleson, E. M. et al. Behavioral context of call production by eastern North Pacific blue whales. Mar. Ecol. Prog. Ser. 330, 269–284 (2007).

5.          McDonald, M. A. An acoustic survey of baleen whales off Great Barrier Island, New Zealand. New Zeal. J. Mar. Freshw. Res. 40, 519–529 (2006).


Vaquita: a porpoise caught between people and money

By: Alexa Kownacki, Ph.D. Student, OSU Department of Fisheries and Wildlife, Geospatial Ecology of Marine Megafauna Lab

When I first learned of the critically endangered vaquita in early 2015, there were an estimated 97 individuals remaining as reported by CIRVA* (Morell 2014). I was a recent graduate with a bachelor’s degree in Wildlife, Fish, and Conservation Biology, and I, of all people, had never heard of the vaquita. Today, there are an estimated 19 vaquita left (Roth 2019).

Digital painting of a vaquita mother with her calf (Image Source: Aquarium of the Pacific).

The vaquita (Phocoena sinus) is a small porpoise endemic to the Sea of Cortez in the northern region of the Gulf of California, Mexico. It is the most endangered marine mammal and has been for many years, and yet, I had not heard of the vaquita. It wasn’t until I listened to a lunchtime seminar hosted by NOAA Fisheries, that I heard about the porpoise. As a young scientist, “in the field”, I was shocked to realize that I was just learning about an animal, let alone a cetacean, actively going extinct in my lifetime. I believe it’s our job to inform those around us of news in our expertise, and I had failed. I wasn’t informed. As much as I tried in the past four years to describe the decline of the smallest cetacean to anyone who’d listen, I was only reaching a few people at a time. But, today, the vaquita is finally capturing the public’s eye thanks to celebrity support and a feature-length film.

A rare photo of a vaquita (Image Source: Tom Jefferson via the Marine Mammal Center)

From executive producer, Leonardo DiCaprio, comes the Sundance Film Festival Audience Award winner, “Sea of Shadows”. The story of the vaquita truly is an “eco-thriller” and one worth watching. This is not your typical plot line of an endangered species tragically going extinct without action. The vaquita’s story boasts big-name players, such as the Mexican Navy, internationally recognized scientists, Mexican cartels, Chinese mafia, celebrities, the National Marine Mammal Foundation, and Sea Shepherd. At the center of this documentary is the elusive vaquita. The vaquita is not hunted, in fact, this species is not desirable for fisherman. The animal is not aggressive and, in contrast, is notoriously shy, only surfacing to breathe. Furthermore, its name roughly translates into “little cow” because of the rings around its eyes and its docile nature. So, why is this cute creature on the road to extinction? The answer: the wrong place at the wrong time.

“Sea of Shadows” official trailer by National Geographic

The vaquita occupy a small part of the Sea of Cortez where totoaba (Totoaba macdonaldi), a large fish in the drum family, is also endemic. If you’re wondering what a small porpoise and a large fish have in common, then you’d be close to recognizing that is the key to understanding this tragedy. Both species are roughly the same size, one to two meters in length with similar girths. The totoaba, although said to have tender meat, is caught for only one organ: the swim bladder. Now referred to as the “cocaine of the sea”, the dried swim bladders of the totoaba are sold to Mexican cartels who then export the product to China. Once in China, illegal markets sell the swim bladders for up to $100,000USD. Unfortunately, the nets used to illegally catch totoaba, also catch the vaquita. The porpoise has no economic value to the fishermen and therefore are tossed as bycatch. The vaquita is the innocent bystander in a war for money and power.

A man displays the catch from an illegal gillnet, including the totoaba in his arms, and a vaquita, below, that was bycatch (Image Source: Omar Vidal via Aquarium of the Pacific/NOAA Fisheries).

Watching a charismatic species severely decline because of human greed is horrific. The film, however, focuses on the effort of a few incredible organizations that band together in the fight to save the vaquita. Moreover, the multimillion-dollar project, Vaquita CPR, is still ongoing. On a more positive note, in October of 2019, scientists spotted six vaquita during continued conservation and monitoring efforts (Blust & Desk 2019). The path to saving a critically endangered species, especially one that is thought not to do well in captivity, is challenging. The vaquita’s recovery path has many complicated connections which for what appears to be an uphill battle. But, we, the people, are responsible for this. We must support research and conservation by using our voice to share what is happening, for a porpoise and for the world.

*Comité Internacional para la Recuperación de la Vaquita (International Committee for the Recovery of the Vaquita)

Citations:

Blust, Kendal, and Fronteras Desk. “Photo Sparks Increased Concern over Fishing in Vaquita Refuge.” Arizona Public Media, 25 Oct. 2019, https://news.azpm.org/p/news-topical-nature/2019/10/25/160806-photo-sparks-increased-concern-over-fishing-in-vaquita-refuge/.

Morell, Virginia. “Vaquita Porpoise Faces Imminent Extinction-Can It Be Saved?” National Geographic, 15 Aug. 2014, https://www.nationalgeographic.com/news/2014/8/140813-vaquita-gulf-california-mexico-totoaba-gillnetting-china-baiji/.

Roth, Annie. “The ‘Little Cow’ of the Sea Nears Extinction.” National Geographic, 17 Sept. 2019, https://www.nationalgeographic.com/animals/2019/09/vaquita-the-porpoise-familys-smallest-member-nears-extinction/#close.

Can sea otters help kelp under a changing climate?

By Dominique Kone1 and Sara Hamilton2

1Masters Student in Marine Resource Management, 2Doctoral Student in Integrative Biology

Five years ago, the North Pacific Ocean experienced a sudden increase in sea surface temperature (SST), known as the warm blob, which altered marine ecosystem function and structure (Leising et al. 2015). Much research illustrated how the warm blob impacted pelagic ecosystems, with relatively less focused on the nearshore environment. Yet, a new study demonstrated how rising ocean temperatures have partially led to bull kelp loss in northern California. Unfortunately, we are once again observing similar warming trends, representing the second largest marine heatwave over recent decades, and signaling the potential rise of a second warm blob. Taken together, all these findings could forecast future warming-related ecosystem shifts in Oregon, highlighting the need for scientists and managers to consider strategies to prevent future kelp loss, such as reintroducing sea otters.

In northern California, researchers observed a dramatic ecosystem shift from productive bull kelp forests to purple sea urchin barrens. The study, led by Dr. Laura Rogers-Bennett from the University of California, Davis and California Department of Fish and Wildlife, determined that this shift was caused by multiple climatic and biological stressors. Beginning in 2013, sea star populations were decimated by sea star wasting disease (SSWD). Sea stars are a main predator of urchins, causing their absence to release purple urchins from predation pressure. Then, starting in 2014, ocean temperatures spiked with the warm blob. These two events created nutrient-poor conditions, which limited kelp growth and productivity, and allowed purple urchin populations to grow unchecked by predators and increase grazing on bull kelp. The combined effect led to approximately 90% reductions in bull kelp, with a reciprocal 60-fold increase in purple urchins (Figure 1).

Figure 1. Kelp loss and ecosystem shifts in northern California (Rogers-Bennett & Catton 2019).

These changes have wrought economic challenges as well as ecological collapse in Northern California. Bull kelp is important habitat and food source for several species of economic importance including red abalone and red sea urchins (Tegner & Levin 1982). Without bull kelp, red abalone and red sea urchin populations have starved, resulting in the subsequent loss of the recreational red abalone ($44 million) and commercial red sea urchin fisheries in Northern California. With such large kelp reductions, purple urchins are also now in a starved state, evidenced by noticeably smaller gonads (Rogers-Bennett & Catton 2019).

Biogeographically, southern Oregon is very similar to northern California, as both are composed of complex rocky substrates and shorelines, bull kelp canopies, and benthic macroinvertebrates (i.e. sea urchins, abalone, etc.). Because Oregon was also impacted by the 2014-2015 warm blob and SSWD, we might expect to see a similar coastwide kelp forest loss along our southern coastline. The story is more complicated than that, however. For instance, ODFW has found purple urchin barrens where almost no kelp remains in some localized places. The GEMM Lab has video footage of purple urchins climbing up kelp stalks to graze within one of these barrens near Port Orford, OR (Figure 2, left). In her study, Dr. Rogers-Bennett explains that this aggressive sea urchin feeding strategy is potentially a sign of food limitation, where high-density urchin populations create intense resource competition. Conversely, at sites like Lighthouse Reef (~45 km from Port Orford) outside Charleston, OR, OSU and University of Oregon divers are currently seeing flourishing bull kelp forests. Urchins at this reef have fat, rich gonads, which is an indicator of high-quality nutrition (Figure 2, right).

Satellites can detect kelp on the surface of the water, giving scientists a way to track kelp extent over time. Preliminary results from Sara Hamilton’s Ph.D. thesis research finds that while some kelp forests have shrunk in past years, others are currently bigger than ever in the last 35 years. It is not clear what is driving this spatial variability in urchin and kelp populations, nor why southern Oregon has not yet faced the same kind of coastwide kelp forest collapse as northern California. Regardless, it is likely that kelp loss in both northern California and southern Oregon may be triggered and/or exacerbated by rising temperatures.

Figure 2. Left: Purple urchin aggressive grazing near Port Orford, OR (GEMM Lab 2019). Right: Flourishing bull kelp near Charleston, OR (Sara Hamilton 2019).

The reintroduction of sea otters has been proposed as a solution to combat rising urchin populations and bull kelp loss in Oregon. From an ecological perspective, there is some validity to this idea. Sea otters are a voracious urchin predator that routinely reduce urchin populations and alleviate herbivory on kelp (Estes & Palmisano 1974). Such restoration and protection of bull kelp could help prevent red abalone and red sea urchin starvation. Additionally, restoring apex predators and increasing species richness is often linked to increased ecosystem resilience, which is particularly important in the face of global anthropogenic change (Estes et al. 2011)

While sea otters could alleviate grazing pressure on Oregon’s bull kelp, this idea only looks at the issue from a top-down, not bottom-up, perspective. Sea otters require a lot of food (Costa 1978, Reidman & Estes 1990), and what they eat will always be a function of prey availability and quality (Ostfeld 1982). Just because urchins are available, doesn’t mean otters will eat them. In fact, sea otters prefer large and heavy (i.e. high gonad content) urchins (Ostfeld 1982). In the field, researchers have observed sea otters avoiding urchins at the center of urchin barrens (personal communication), presumably because those urchins have less access to kelp beds than on the barren periphery, and therefore, are constantly in a starved state (Konar & Estes 2003) (Figure 3). These findings suggest prey quality is more important to sea otter survival than just prey abundance.

Figure 3. Left: Sea urchin barren (Annie Crawley). Right: Urchin gonads (Sea to Table).

Purple urchin quality has not been widely assessed in Oregon, but early results show that gonad size varies widely depending on urchin density and habitat type. In places where urchin barrens have formed, like Port Orford, purple urchins are likely starving and thus may be a poor source of nutrition for sea otters. Before we decide whether sea otters are a viable tool to combat kelp loss, prey surveys may need to be conducted to assess if a sea otter population could be sustained based on their caloric requirements. Furthermore, predictions of how these prey populations may change due to rising temperatures could help determine the potential for sea otters to become reestablished in Oregon under rapid environmental change.

Recent events in California could signal climate-driven processes that are already impacting some parts of Oregon and could become more widespread. Dr. Rogers-Bennett’s study is valuable as she has quantified and described ecosystem changes that might occur along Oregon’s southern coastline. The resurgence of a potential second warm blob and the frequency between these warming events begs the question if such temperature spikes are still anomalous or becoming the norm. If the latter, we could see more pronounced kelp loss and major shifts in nearshore ecosystem baselines, where function and structure is permanently altered. Whether reintroducing sea otters can prevent these changes will ultimately depend on prey and habitat availability and quality, and should be carefully considered.

References:

Costa, D. P. 1978. The ecological energetics, water, and electrolyte balance of the California sea otter (Enhydra lutris). Ph.D. dissertation, University of California, Santa Cruz.

Estes, J. A. and J.F. Palmisano. 1974. Sea otters: their role in structuring nearshore communities. Science. 185(4156): 1058-1060.

Estes et al. 2011. Trophic downgrading of planet Earth. Science. 333(6040): 301-306.

Harvell et al. 2019. Disease epidemic and a marine heat wave are associated with the continental-scale collapse of a pivotal predator (Pycnopodia helianthoides). Science Advances. 5(1).

Konar, B., and J. A. Estes. 2003. The stability of boundary regions between kelp beds and deforested areas. Ecology. 84(1): 174-185.

Leising et al. 2015. State of California Current 2014-2015: impacts of the warm-water “blob”. CalCOFI Reports. (56): 31-68.

Ostfeld, R. S. 1982. Foraging strategies and prey switching in the California sea otter. Oecologia. 53(2): 170-178.

Reidman, M. L. and J. A. Estes. 1990. The sea otter (Enhydra lutris): behavior, ecology, and natural history. United States Department of the Interior, Fish and Wildlife Service, Biological Report. 90: 1-126.

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

Tegner, M. J., and L. A. Levin. 1982. Do sea urchins and abalones compete in California? International Echinoderms Conference, Tampa Bay. J. M Lawrence, ed.