Marine megafauna as ecosystem sentinels: What animals can tell us about changing oceans

By Dawn Barlow1 and Will Kennerley2

1PhD Candidate, OSU Department of Fisheries, Wildlife, and Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

2MS Student, OSU Department of Fisheries, Wildlife, and Conservation Sciences, Seabird Oceanography Lab

The marine environment is dynamic, and mobile animals must respond to the patchy and ephemeral availability of resource in order to make a living (Hyrenbach et al. 2000). Climate change is making ocean ecosystems increasingly unstable, yet these novel conditions can be difficult to document given the vast depth and remoteness of most ocean locations. Marine megafauna species such as marine mammals and seabirds integrate ecological processes that are often difficult to observe directly, by shifting patterns in their distribution, behavior, physiology, and life history in response to changes in their environment (Croll et al. 1998, Hazen et al. 2019). These mobile marine animals now face additional challenges as rising temperatures due to global climate change impact marine ecosystems worldwide (Hazen et al. 2013, Sydeman et al. 2015, Silber et al. 2017, Becker et al. 2019). Given their mobility, visibility, and integration of ocean processes across spatial and temporal scales, these marine predator species have earned the reputation as effective ecosystem sentinels. As sentinels, they have the capacity to shed light on ecosystem function, identify risks to human health, and even predict future changes (Hazen et al. 2019). So, let’s explore a few examples of how studying marine megafauna has revealed important new insights, pointing toward the importance of monitoring these sentinels in a rapidly changing ocean.

Cairns (1988) is often credited as first promoting seabirds as ecosystem sentinels and noted several key reasons why they were perfect for this role: (1) Seabirds are abundant, wide-ranging, and conspicuous, (2) although they feed at sea, they must return to land to nest, allowing easier observation and quantification of demographic responses, often at a fraction of the cost of traditional, ship-based oceanographic surveys, and therefore (3) parameters such as seabird reproductive success or activity budgets may respond to changing environmental conditions and provide researchers with metrics by which to assess the current state of that ecosystem.

The unprecedented 2014-2016 North Pacific marine heatwave (“the Blob”) caused extreme ecosystem disruption over an immense swath of the ocean (Cavole et al. 2016). Seabirds offered an effective and morbid indication of the scale of this disruption: Common murres (Uria aalge), an abundant and widespread fish-eating seabird, experienced widespread breeding failure across the North Pacific. Poor reproductive performance suggested that there may have been fewer small forage fish around and that these changes occurred at a large geographic scale. The Blob reached such an extreme as to kill immense numbers of adult birds, which professional and community scientists found washed up on beach-surveys; researchers estimate that an incredible 1,200,000 murres may have died from starvation during this period (Piatt et al. 2020). While the average person along the Northeast Pacific Coast during this time likely didn’t notice any dramatic difference in the ocean, seabirds were shouting at us that something was terribly wrong.

Happily, living seabirds also act as superb ecosystem sentinels. Long-term research in the Gulf of Maine by U.S. and Canadian scientists monitors the prey species provisioned by adult seabirds to their chicks. Will has spent countless hours over five summers helping to conduct this research by watching terns (Sterna spp.) and Atlantic puffins (Fratercula arctica) bring food to their young on small islands off the Maine coast. After doing this work for multiple years, it’s easy to notice that what adults feed their chicks varies from year to year. It was soon realized that these data could offer insight into oceanographic conditions and could even help managers assess the size of regional fish stocks. One of the dominant prey species in this region is Atlantic herring (Clupea harengus), which also happens to be the focus of an economically important fishery.  While the fishery targets four or five-year-old adult herring, the seabirds target smaller, younger herring. By looking at the relative amounts and sizes of young herring collected by these seabirds in the Gulf of Maine, these data can help predict herring recruitment and the relative number of adult herring that may be available to fishers several years in the future (Scopel et al. 2018).  With some continued modelling, the work that we do on a seabird colony in Maine with just a pair of binoculars can support or maybe even replace at least some of the expensive ship-based trawl surveys that are now a popular means of assessing fish stocks.

A common tern (Sterna hirundo) with a young Atlantic herring from the Gulf of Maine, ready to feed its chick (Photo courtesy of the National Audubon Society’s Seabird Institute)

For more far-ranging and inaccessible marine predators such as whales, measuring things such as dietary shifts can be more challenging than it is for seabirds. Nevertheless, whales are valuable ecosystem sentinels as well. Changes in the distribution and migration phenology of specialist foragers such as blue whales (Balaenoptera musculus) and North Atlantic right whales (Eubalaena glacialis) can indicate relative changes in the distribution and abundance of their zooplankton prey and underlying ocean conditions (Hazen et al. 2019). In the case of the critically endangered North Atlantic right whale, their recent declines in reproductive success reflect a broader regime shift in climate and ocean conditions. Reduced copepod prey has resulted in fewer foraging opportunities and changing foraging grounds, which may be insufficient for whales to obtain necessary energetic stores to support calving (Gavrilchuk et al. 2021, Meyer-Gutbrod et al. 2021). These whales assimilate and showcase the broad-scale impacts of climate change on the ecosystem they inhabit.

Blue whales that feed in the rich upwelling system off the coast of California rely on the availability of their krill prey to support the population (Croll et al. 2005). A recent study used acoustic monitoring of blue whale song to examine the timing of annual population-level transition from foraging to breeding migration compared to oceanographic variation, and found that flexibility in timing may be a key adaptation to persistence of this endangered population facing pressures of rapid environmental change (Oestreich et al. 2022). Specifically, blue whales delayed the transition from foraging to breeding migration in years of the highest and most persistent biological productivity from upwelling, and therefore listening to the vocalizations of these whales may be valuable indicator of the state of productivity in the ecosystem.

Figure reproduced from Oestreich et al. 2022, showing relationships between blue whale life-history transition and oceanographic phenology of foraging habitat. Timing of the behavioral transition from foraging to migration (day of year on the y-axis) is compared to (a) the date of upwelling onset; (b) the date of peak upwelling; and (c) total upwelling accumulated from the spring transition to the end of the upwelling season.

In a similar vein, research by the GEMM Lab on blue whale ecology in New Zealand has linked their vocalizations known as D calls to upwelling conditions, demonstrating that these calls likely reflect blue whale foraging opportunities (Barlow et al. 2021). In ongoing analyses, we are finding that these foraging-related calls were drastically reduced during marine heatwave conditions, which we know altered blue whale distribution in the region (Barlow et al. 2020). Now, for the final component of Dawn’s PhD, she is linking year-round environmental conditions to the occurrence patterns of different blue whale vocalization types, hoping to shed light on ecosystem processes by listening to the signals of these ecosystem sentinels.

A blue whale comes up for air in the South Taranaki Bight of New Zealand. photo by L. Torres.

It is important to understand the widespread implications of the rapidly warming climate and changing ocean conditions on valuable and vulnerable marine ecosystems. The cases explored here in this blog exemplify the importance of monitoring these marine megafauna sentinel species, both now and into the future, as they reflect the health of the ecosystems they inhabit.

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References:

Barlow DR, Bernard KS, Escobar-Flores P, Palacios DM, Torres LG (2020) Links in the trophic chain: Modeling functional relationships between in situ oceanography, krill, and blue whale distribution under different oceanographic regimes. Mar Ecol Prog Ser 642:207–225.

Barlow DR, Klinck H, Ponirakis D, Garvey C, Torres LG (2021) Temporal and spatial lags between wind, coastal upwelling, and blue whale occurrence. Sci Rep 11:1–10.

Becker EA, Forney KA, Redfern J V., Barlow J, Jacox MG, Roberts JJ, Palacios DM (2019) Predicting cetacean abundance and distribution in a changing climate. Divers Distrib 25:626–643.

Cairns DK (1988) Seabirds as indicators of marine food supplies. Biol Oceanogr 5:261–271.

Cavole LM, Demko AM, Diner RE, Giddings A, Koester I, Pagniello CMLS, Paulsen ML, Ramirez-Valdez A, Schwenck SM, Yen NK, Zill ME, Franks PJS (2016) Biological impacts of the 2013–2015 warm-water anomaly in the northeast Pacific: Winners, losers, and the future. Oceanography 29:273–285.

Croll DA, Marinovic B, Benson S, Chavez FP, Black N, Ternullo R, Tershy BR (2005) From wind to whales: Trophic links in a coastal upwelling system. Mar Ecol Prog Ser 289:117–130.

Croll DA, Tershy BR, Hewitt RP, Demer DA, Fiedler PC, Smith SE, Armstrong W, Popp JM, Kiekhefer T, Lopez VR, Urban J, Gendron D (1998) An integrated approch to the foraging ecology of marine birds and mammals. Deep Res Part II Top Stud Oceanogr.

Gavrilchuk K, Lesage V, Fortune SME, Trites AW, Plourde S (2021) Foraging habitat of North Atlantic right whales has declined in the Gulf of St. Lawrence, Canada, and may be insufficient for successful reproduction. Endanger Species Res 44:113–136.

Hazen EL, Abrahms B, Brodie S, Carroll G, Jacox MG, Savoca MS, Scales KL, Sydeman WJ, Bograd SJ (2019) Marine top predators as climate and ecosystem sentinels. Front Ecol Environ 17:565–574.

Hazen EL, Jorgensen S, Rykaczewski RR, Bograd SJ, Foley DG, Jonsen ID, Shaffer SA, Dunne JP, Costa DP, Crowder LB, Block BA (2013) Predicted habitat shifts of Pacific top predators in a changing climate. Nat Clim Chang 3:234–238.

Hyrenbach KD, Forney KA, Dayton PK (2000) Marine protected areas and ocean basin management. Aquat Conserv Mar Freshw Ecosyst 10:437–458.

Meyer-Gutbrod EL, Greene CH, Davies KTA, Johns DG (2021) Ocean regime shift is driving collapse of the north atlantic right whale population. Oceanography 34:22–31.

Oestreich WK, Abrahms B, Mckenna MF, Goldbogen JA, Crowder LB, Ryan JP (2022) Acoustic signature reveals blue whales tune life history transitions to oceanographic conditions. Funct Ecol.

Piatt JF, Parrish JK, Renner HM, Schoen SK, Jones TT, Arimitsu ML, Kuletz KJ, Bodenstein B, Garcia-Reyes M, Duerr RS, Corcoran RM, Kaler RSA, McChesney J, Golightly RT, Coletti HA, Suryan RM, Burgess HK, Lindsey J, Lindquist K, Warzybok PM, Jahncke J, Roletto J, Sydeman WJ (2020) Extreme mortality and reproductive failure of common murres resulting from the northeast Pacific marine heatwave of 2014-2016. PLoS One 15:e0226087.

Scopel LC, Diamond AW, Kress SW, Hards AR, Shannon P (2018) Seabird diets as bioindicators of atlantic herring recruitment and stock size: A new tool for ecosystem-based fisheries management. Can J Fish Aquat Sci.

Silber GK, Lettrich MD, Thomas PO, Baker JD, Baumgartner M, Becker EA, Boveng P, Dick DM, Fiechter J, Forcada J, Forney KA, Griffis RB, Hare JA, Hobday AJ, Howell D, Laidre KL, Mantua N, Quakenbush L, Santora JA, Stafford KM, Spencer P, Stock C, Sydeman W, Van Houtan K, Waples RS (2017) Projecting marine mammal distribution in a changing climate. Front Mar Sci 4:413.

Sydeman WJ, Poloczanska E, Reed TE, Thompson SA (2015) Climate change and marine vertebrates. Science 350:772–777.

Social turmoil due to the approval of an offshore oil exploration project off the coast of Argentina.

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

I just returned to my home country, Argentina, after over 2 years without leaving the USA due to COVID-19 travel restrictions. Being back with my family, my friends, my culture, and speaking my native language feels great and relaxing. However, I returned to a country struggling to rebound from the coronavirus pandemic. I am afraid this post pandemic scenario places Argentina in a vulnerable situation. The need for economic growth could result in decisions or policies that, in the long term, hurt the country, leaving environmental damage for potential economic growth.

Argentina holds extensive oil and gas deposits, including the world’s second largest gas formation, Vaca Muerta. Although offshore (i.e., in the ocean) oil exploration and exploitation are not yet extensively developed, the intention of offshore gas and oil drilling is on the agenda. In July 2021, a public hearing was held with the purpose to consider the environmental impact assessment for carrying out seismic exploration in the North Argentinian basin off the southern coast of the Buenos Aires province. Over 90% of the participants, including scientists, researchers, technicians from various institutions, non-governmental organizations and representatives of the fishing sector spoke against the project and highlighted the negative impacts that such activity can generate on marine life, and to other socioeconomic activities such as tourism and fishing, not only in Argentina but at the regional level.

Thousands of people marched along the beaches and the main coastal cities of Argentina to protest against the approval for a seismic explorations project in the Argentinian basin. Photo source: prensaobrera.com

Seismic prospections are usually done with the purpose for oil and gas exploitation and less frequently for research purposes. In seismic prospections, ships carry out explosions with airguns, whose sound waves reach the seabed, bounce back and are captured by receivers on the ships to map the petroleum deposits in seafloor and identify potential areas for hydrocarbon extractions. The sound emitted by the seismic airguns can reach extremely loud levels of sounds that travel for thousands of miles underwater. Such extreme high levels of sound can alter the behavior of many marine species, from the smallest planktonic species, to the largest marine mammals, masking their communication, causing physical and physiological stress, interfering with their vital functions, and reducing the local availability of prey (Di Iorio & Clark, 2010; Hildebrand, 2009; Weilgart, 2018).

Here you can listen to a short audio clip of a seismic airgun firing every ~8 seconds, a typical pattern. Close your eyes and imagine you are a whale living in this environment. Now, put the clip on loop and play it for three months straight. This would be the soundscape that whales living in a region of oil and gas exploration hear, as seismic surveys often last 1-4 months (see our previous post “Hearing is believing” for more details).

Despite the public rejection and the mounting evidence about the negative impacts and environmental risks associated with such activities, the government approved the initiation of the seismic prospection off the southern coast of Buenos Aires. In response, thousands of people marched along the beaches and the main coastal cities of Argentina to protest against the oil exploration project. The areas where the seismic surveys will be carried out overlap largely with the southern right whale’s migration routes and feeding areas during their spring and summer (Figure 1). Likewise, the area overlaps with highly productive areas in the ocean that hosts great biodiversity of species of ecological and commercial importance, including the feeding areas of seabirds, turtles and other marine mammals. Additionally, the seismic activity will endanger the health of the beaches of the coast of Buenos Aires and Uruguay where thousands of tourists spend the summer to escape from the large cities.

Figure 1. The map on the left is showing (light blue squares CAN_100, CAN_108, and CAN_114) the areas where seismic prospections are proposes. The map on the right is showing the individual satellite track lines for eleven individual southern right whales (SRW) during the feeding season. You can observe that the proposed area for seismic explorations overlaps with critical feeding habitat for the SRW. Source: Whale Conservation Institute of Argentina (ICB).

The impacts of these activities to marine wildlife are difficult to control and monitor (Elliott et al. 2019, Gordon et al, 2003), especially for large whales that are a very challenging taxa to study (Hunt et al. 2013). We know that the ability to perceive biologically important sounds is critical to marine mammals, and acoustic disturbance through human-generated noise can interfere with their natural functions. Sounds from seismic surveys are intense and have peak frequency bands overlapping those used by baleen whales (Di Lorio & Clark, 2010); however, evidence of interference with baleen whale acoustic communication, and the effects on their health and physiology are sparse. In this context, the GEMM Lab project GRANITE (Gray Whale Response to Ambient Noise Informed by Technology and Ecology), plans to generate information to fulfill these knowledge gaps and provide tools to aid conservation and management decisions in terms of allowable noise level in whale habitats. I am hopeful such information will reach decision makers and influence their decisions, however, sometimes it is frustrating to see how evidence-based information generated with high quality standards are often ignored.

The recent approval of the seismic exploration in Argentina is an example of my frustration. There is no way that the oil industry can guarantee a low-risk of impact on biodiversity and the environment. There are too many examples of environmental catastrophes related to the oil industries at sea that speak for themselves. Moreover, the promotion of such activities goes against the compromises assumed by the country to work to mitigate the effects of Climate Change, and to achieve the reductions of the greenhouse gas emissions to comply with the Paris Agreement. Decades of research help recognized the areas that would be impacted by these seismic activities as key habitat for the life cycle of whales, penguins, seals and more. But, apparently all these scientific data are ignored at the time of weighing the tradeoffs between “economic development” and environmental impacts. As a conservation biologist, I am questioning what can be done in order to be heard and significantly influence such decisions.

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References:

  • Di Iorio, L., & Clark, C. W. (2010). Exposure to seismic survey alters blue whale acoustic communication. Biology Letters, 6(1), 51–54. https://doi.org/10.1098/rsbl.2009.0651
  • Weilgart, L. (2018). The impact of ocean noise pollution on fish and invertebrates. Report for OceanCare, Switzerland.
  • Elliott, B. W., Read, A. J., Godley, B. J., Nelms, S. E., & Nowacek, D. P. (2019). Critical information gaps remain in understanding impacts of industrial seismic surveys on marine vertebrates. In Endangered Species Research (Vol. 39, pp. 247–254). Inter-Research. https://doi.org/10.3354/esr00968
  • Gordon, J., Gillespie, D., Potter, J., Frantzis, A., Simmonds, M. P., Swift, R., & Thompson, D. (2003). A review of the effects of seismic surveys on marine mammals. Marine Technology Society Journal37(4), 16-34.
  • Hunt, K. E., Moore, M. J., Rolland, R. M., Kellar, N. M., Hall, A. J., Kershaw, J., Raverty, S. A., Davis, C. E., Yeates, L. C., Fauquier, D. A., Rowles, T. K., & Kraus, S. D. (2013). Overcoming the challenges of studying conservation physiology in large whales: a review of available methods. Conservation Physiology, cot006–cot006. https://doi.org/10.1093/conphys/cot006

Of snakes and whales: How food availability and body condition affect reproduction

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

Over six field seasons the GEMM lab team has conducted nearly 500 drone flights over gray whales, equaling over 100 hours of footage. These hours of footage are the central dataset for my PhD dissertation, so it’s up to me to process them all. This process can be challenging, tedious, and daunting, but it is also quite fun and a privilege to be the one person who gets to watch all the footage. It’s fascinating to get to know the whales and their behaviors and pick up on patterns. It motivates me to get through this video processing step and start doing the data analysis. Recently, it’s been especially fun to notice patterns that I’ve seen mentioned in the literature. One example is adult social behavior. 

There are two categories of social behavior that I’m interested in studying: maternal behavior, defined as interactions between a mom and its calf, and general social behaviors, defined as social interactions between non-mom/calf pairs. In this blog I’ll focus on general social behaviors, but if you’re interested in maternal behavior check out this blog. General social behavior, which I’ll refer to as social behavior moving forward, includes tactile interactions and promiscuous behaviors (Torres et al. 2018; Clip 1). While gray whales in the PCFG range are primarily foraging, researchers have observed increases in social behavior towards the end of the foraging season (Stelle et al., 2008; Torres et al., 2018). We think that this indicates that the whales are starting to focus less on feeding and more on breeding. This tradeoff of foraging vs. socializing time is interesting because it comes at an energetic cost.

Clip 1. Example of social interaction between a male and female gray whale off the coast of Oregon, USA. Collected under NOAA/NMFS permit #21678

Broadly, animals need to balance the energetic demands of survival with those of reproduction. They need to reproduce to pass on their genes, but reproduction is energetically demanding, and animals also need to survive and grow to be able to reproduce. The decision to reproduce is costly because reproduction requires energetic investment and time investment since animals do not forage (gaining energy) when they are socializing. Consequently, only animals with sufficient energy reserves (i.e., body condition) to invest in reproduction actually engage in reproduction. Given these costs associated with reproduction, we expect to see a relationship between social behavior and body condition (Green, 2001) with mainly animals in good body condition engaging in social behavior because these animals have sufficient reserves to sustain the cost. Furthermore, since body condition is an indicator of foraging success and prey availability, environmental conditions can also affect social behavior and reproduction through this pathway. 

Rahman et al. (2014) used a lab experiment to study the relationship between nutritional stress and male guppy courtship behavior (Figure 1). In their experiment they tested for the effects of both decreased diet quantity and quality on the frequency of male courtship behaviors. Rahman et al (2014) found that individuals in the low-quantity group were significantly smaller than those in the high-quality group and that diet quantity had a significant effect on the frequency of courtship behaviors. Males fed a low-quantity diet performed fewer courtship behaviors. Interestingly, there was no significant effect of diet quality on courtships behavior, although there was some evidence of an interaction effect, which suggests that within the low-quantity group, males fed with high-quality food performed more courtship behaviors that those fed with low-quality food. This study is interesting because it shows how foraging success (diet quantity and quality) can affect courting behavior. 

Figure 1. A guppy (Rahman et al., 2013)

However, guppies are not the ideal species for comparison to gray whales because gray whales and guppies have quite different life history traits. A more fitting comparison would be with an example species with more in common with gray whales, such as viviparous capital breeders. Viviparous animals develop the embryo inside the body and give live birth. Capital breeders forage to build energy reserves and then rely on those energy reserves during reproduction. Surprisingly, I found asp vipers to be a good example species for comparison to gray whales.

Asp vipers (Figure 2) are viviparous snakes who are considered capital breeders because they forage prior to hibernation, and then begin reproduction immediately following hibernation without additional foraging. Naulleau & Bonnet (1996) conducted a field study on female asp vipers to determine if there was a difference in body condition at the start of the breeding season between females who reproduced or not during that season. To do this they marked individuals and measured their body condition at the start of the breeding season and then recaptured those individuals at the end of the breeding season and recorded whether the individual had reproduced. Interestingly, they found that there was a strongly significant difference in body condition between females that did and did not reproduce. In fact, they discovered that no female below a certain body condition value reproduced, meaning that they found a body condition threshold for reproduction. 

Figure 2. An asp viper

Additionally, a study on water pythons found that their body condition threshold for reproduction shifted over time in response to prey availability (Madsen & Shine, 1999). These authors found that females lowered their threshold after several consecutive years of poor prey availability. These studies are really exciting to me because they address questions that the GRANITE project team is interested in tackling.

Understanding the relationship between body condition and reproduction in gray whales is an important puzzle piece for our work. The aim of the GRANITE project is to understand how the effects of stressors on individual whales scales up to population level impacts (read Lisa’s blog to learn more). Reproduction rates play a big role in population dynamics, so it is important to understand what factors affect reproduction. Since we’re studying these whales on their foraging grounds, assessing body condition provides an important link between foraging behavior and reproduction. 

For example, if an individual’s response to a stressor is to forage less, that may lead to poorer body condition, meaning that they may be less likely to reproduce. While reduced reproduction in one individual may not have a big effect on the population, the same response from multiple individuals could impact the population’s dynamics (i.e., increasing or decreasing abundance). Understanding these different relationships between behavior, body condition, and reproduction rates is a big undertaking, but it’s exciting to be a member of the GRANITE team as this strong group of scientists works to bring together different data streams to work on this big picture question. We’re all deep into data processing right now so stay tuned over the next few years to learn more about gray whale social behavior and to find out if fat whales are more social than skinny whales. 

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References

Green, A. J. (2001). Mass/Length Residuals: Measures of Body Condition or Generators of Spurious Results? Ecology82(5), 1473–1483. https://doi.org/10.1890/0012-9658(2001)082[1473:MLRMOB]2.0.CO;2

Madsen, T., & Shine, R. (1999). The adjustment of reproductive threshold to prey abundance in a capital breeder. Journal of Animal Ecology68(3), 571–580. https://doi.org/10.1046/j.1365-2656.1999.00306.x

Naulleau, G., & Bonnet, X. (1996). Body Condition Threshold for Breeding in a Viviparous Snake. Oecologia107(3), 301–306.

Rahman, M. M., Kelley, J. L., & Evans, J. P. (2013). Condition-dependent expression of pre- and postcopulatory sexual traits in guppies. Ecology and Evolution3(7), 2197–2213. https://doi.org/10.1002/ece3.632

Rahman, M. M., Turchini, G. M., Gasparini, C., Norambuena, F., & Evans, J. P. (2014). The Expression of Pre- and Postcopulatory Sexually Selected Traits Reflects Levels of Dietary Stress in Guppies. PLOS ONE9(8), e105856. https://doi.org/10.1371/journal.pone.0105856

Stelle, L. L., Megill, W. M., & Kinzel, M. R. (2008). Activity budget and diving behavior of gray whales (Eschrichtius robustus) in feeding grounds off coastal British Columbia. Marine Mammal Science24(3), 462–478. https://doi.org/10.1111/j.1748-7692.2008.00205.x

Torres, L. G., Nieukirk, S. L., Lemos, L., & Chandler, T. E. (2018). Drone up! Quantifying whale behavior from a new perspective improves observational capacity. Frontiers in Marine Science5(SEP). https://doi.org/10.3389/fmars.2018.00319

Let me introduce you to… dugongs!

By Solène Derville, Postdoc, OSU Department of Fisheries, Wildlife, and Conservation Science, Geospatial Ecology of Marine Megafauna Lab

Today let me take you on a journey into the tropical waters of the Indo-Pacific Ocean, far from Oregon’s beautiful coasts. Although I have been working as a postdoc on the OPAL project for a year, the pandemic has prevented me from moving to the US as planned. Like so many around the globe, I have been working remotely from my study area (Oregon coastal waters), imagining my study species (blue, fin and humpback whales) gently swimming and feeding along the productive California Current system. One day, I’ll get to see these amazing animals for real, that’s for sure.

But in the meantime, I have taken this year as an opportunity to work with the GEMM lab, while continuing to enjoy the marvels of New Caledonia, a French overseas territory where I have lived for more than 6 years now. Among the animals that I get to approach and observe regularly in the coral reef lagoons that surround the island, the dugong (Dugon dugon) is perhaps the most emblematic and intriguing. This marine mammal is listed as vulnerable in the IUCN Red list of threatened species and has been the focus of important research and conservation efforts in New Caledonia over the last two decades1–3. During my previous post-doctoral position at the French Institute of Research for Sustainable Development, I contributed to some recent research involving satellite tracking of dugongs in the region. This work has led to a publication, now in review4, and will be the topic of my oral presentation at the 7th International Bio-Logging Science Symposium hosted in Hawaii in a couple weeks.

While I was analyzing dugong satellite tracks, writing this paper with my colleagues and preparing for the symposium, I learned a lot about these strange “sea cows”. Dugongs belong to the Sirenian marine mammal order, just like manatees (West Indian, Amazonian and West African species), which they are often mistaken for (watch out: Google Images will misleadingly suggest hundreds of manatee pictures if you make a “dugong” keyword search). The physiology and anatomy of dugongs is actually quite different from that of manatees (Figure 1). They also live in a different part of the world as they are broadly distributed in the Indo-Pacific coastal and island waters. Dugongs form separate populations, some of which are very isolated and at high risk of extirpation. They are found in 37 different countries, with Australia being home to the largest populations by far (exceeding 70,000 individuals5).

Figure 1: Manatee vs Dugong, can you tell them apart? Among other things, dugongs and manatees have a very different body shape. As the famous Sirenian specialist Helene Marsh said, a dugong essentially looks like “a manatee that goes to the gym”5! Illustration by S. Derville.

Sea cow or sea elephant?

Through the tree of evolution, the dugong and manatee’s closest relative is not the one you would think… other marine mammals like cetaceans or pinnipeds. Indeed, molecular genetic analyses have placed the Sirenians in the Afrotheria Superorder of mammals. Therefore, it appears that dugongs are more closely related to elephant and golden moles than to whales and dolphins!

As a memory aid to help remember this ancient origin, we may notice that both elephants and dugongs have tusks. Mature male and female dugongs have erupted tusks, although the females’ only erupt rarely and at a very old age. Interestingly, tusks are used by scientists to determine age. Analyses of growth layers in bisected dugong tusks have revealed that dugongs are long-lived, with a maximum longevity record of 73 years (estimated from a female individual found in Western Australia5).

An (almost) vegetarian marine mammal

Dugongs and manatees are the only predominantly herbivorous aquatic mammals. Given that manatees use both marine and fresh water ecosystems they tend to have a broader diet, eating many kinds of submerged, floating or emergent algae and seagrass (even bank growth!). On the other hand, dugongs are a strictly marine species and primarily feed on seagrass, which may look very similar to seaweeds, but are in fact marine flowering plants. Seagrass tend to form underwater shallow meadows that are among the most productive ecosystems in the world6. In fact, dugong grazing influences the biomass, species composition and nutritional quality of seagrass meadows7,8. Just like we take care of our gardens, dugongs regulate seagrass ecosystems. But there is more. Recent research conducted in the Great Barrier Reef indicates that seagrass seeds that have been digested by dugongs germinate at a faster rate9. As well as playing a role in dispersal10, it appears that dugongs are pooping seeds with enhanced germination potential, hence participating to seagrass meadow resilience.

Figure 2: Dugong mother and calf feeding on a dense seagrass bed (a) and solitary adult foraging in a very sparce seagrass bed (b). Seagrass grows in many different types of meadows, which may vary in density, species composition and substrate. For instance, seagrass species of the Halophila genus are among the preferred dugong’s meals although may be very thinly distributed (c). Photo credit: Serge Andréfouët, New Caledonia.

Unlike manatees, dugongs cannot feed over the whole water column and are strictly bottom feeders. They use their deflected snout (Figure 1) to search the seabed for their favorite food (Figure 2). The feeding trails left by dugongs in dense seagrass meadows are easily detectable from above, just like the sediment clouds that they generate when searching muddy bottoms. Although seagrass is undoubtedly the main component of the dugong’s diet, they may incidentally (or not) ingest algae and invertebrates5.

A legendary animal

The etymology for the word Sirenian comes from the mermaids, or “sirens” of the Greek mythology. These aquatic creatures with the upper body of a female human would sing to lure sailors towards the shore… and towards a certain death. The morphology of dugongs and manatees shares some resemblance with mermaids, at least enough for desperate and lonely sailors to think so!

In addition to having a scientific name rooted in legends, dugongs are also important to contemporary human cultures. In tropical islands and coastal communities, marine megafauna species such as dugongs are considered heritage, due to the strong bond that their people have forged with the ocean5. Dugongs may play an important cultural role because they can be part of the socio-symbolic organization of societies, associated with the imaginary world, or simply because they are seen as companions of the sea, which people frequently encounter. For New Caledonia’s indigenous people, the Kanaks, dugongs can be totem to tribes. Like other large marine species (whales, sharks), the dugong is also considered as an embodiment of ancestors11.

Dugongs have been hunted throughout their range since prehistoric times. Archaeological excavations such as those conducted on the island of Akab in the United Arab Emirates12, indicate that dugong hunting played a role in ancient rituals, in addition to providing a large quantity of meat. The cultural value of dugongs is recognized by multiple countries, which have therefore authorized indigenous dugong hunting, sometimes under quotas. For instance, in Australia, dugongs may be legally hunted by Aboriginal and Torres Strait Islander people (Figure 3) under section 211 of the Native Title Act 1993.

In New Caledonia, the dugong has been protected since 1962 and its hunting is only authorized in one province, with a dispensation for traditional Kanak celebrations13. However, in view of the critical situation in which the New Caledonian dugong population finds itself, estimated at around 700 individuals in 2008-201214, no hunting exemptions have been issued since 2004.

Figure 3: “Naath” (dugong hunting platform), hand colored linocut by Torres Strait Islander artist Dennis Nona. The art piece represents traditional dugong hunting where the hunter is guided by the phosphorescent glow the dugong would leave in the water at night.

What future for dugongs?

Despite legislations to forbid dugong meat consumption outside specific traditional permits, poaching persists, in New Caledonia and in many of the “low-income” countries that are home to dugongs. As climate change and demography intensifies risks to food security, scientists and stakeholders fear for dugongs. Moreover, dugongs entirely rely on seagrass ecosystems that are also disappearing at an alarming rate (7% per year6) as a result of coastal development, pollution and overfishing.

Can we preserve dugongs in regions of high climate vulnerability and where people still have low levels of access to basic needs? Can dugongs play the role of “umbrellas” for the conservation of the ecosystem they live in? I do not have the answer to these questions but I certainly believe that people’s well-being and environmental conservation are tightly intertwined. I hope that rising transdisciplinary approaches such as those supported by the “One Health” framework will help reconnect human populations to their environment, and achieve the goal of optimal health for everyone, humans and animals.

References

1.        Garrigue, C., Patenaude, N. & Marsh, H. Distribution and abundance of the dugong in New Caledonia, southwest Pacific. Mar. Mammal Sci. 24, 81–90 (2008).

2.        Cleguer, C., Grech, A., Garrigue, C. & Marsh, H. Spatial mismatch between marine protected areas and dugongs in New Caledonia. Biol. Conserv. 184, 154–162 (2015).

3.        Cleguer, C., Garrigue, C. & Marsh, H. Dugong (Dugong dugon) movements and habitat use in a coral reef lagoonal ecosystem. Endanger. Species Res. 43, 167–181 (2020).

4.        Derville, S., Cleguer, C. & Garrigue, C. Ecoregional and temporal dynamics of dugong habitat use in a complex coral reef lagoon ecosystem. Sci. Rep. (In review)

5.        Marsh, H., O’Shea, T. J. & Reynolds, J. E. I. Ecology and conservation of the Sirenia: dugongs and manatees, Vol 18. (Cambridge University Press, Cambridge, 2011).

6.        Unsworth, R. K. F. & Cullen-Unsworth, L. C. Seagrass meadows. Curr. Biol. 27, R443–R445 (2017).

7.        Aragones, L. V., Lawler, I. R., Foley, W. J. & Marsh, H. Dugong grazing and turtle cropping: Grazing optimization in tropical seagrass systems? Oecologia 149, 635–647 (2006).

8.        Preen, A. Impacts of dugong foraging on seagrass habitats: observational and experimental evidence for cultivation grazing. Mar. Ecol. Prog. Ser. 124, 201–213 (1995).

9.        Tol, S. J., Jarvis, J. C., York, P. H., Congdon, B. C. & Coles, R. G. Mutualistic relationships in marine angiosperms: Enhanced germination of seeds by mega-herbivores. Biotropica (2021) doi:10.1111/btp.13001.

10.      Tol, S. J. et al. Long distance biotic dispersal of tropical seagrass seeds by marine mega-herbivores. Sci. Rep. 7, 1–8 (2017).

11.      Dupont, A. Évaluation de la place du dugong dans la société néo-calédonienne. (Mémoire Master. Encadré par L. Gardes (Agence des Aires Marines Protégées) et C. Sabinot (IRD), 2015).

12.      Méry, S., Charpentier, V., Auxiette, G. & Pelle, E. A dugong bone mound: The Neolithic ritual site on Akab in Umm al-Quwain, United Arab Emirates. Antiquity 83, 696–708 (2009).

13.      Leblic, I. Vivre de la mer, vivre de la terre… en pays kanak. Savoirs et techniques des pêcheurs kanak du sud de la Nouvelle-Calédonie. (Société des Océanistes, 2008).

14.      Hagihara, R. et al. Compensating for geographic variation in detection probability with water depth improves abundance estimates of coastal marine megafauna. PLoS One 13, e0191476 (2018).

Stories from a whale’s life: how whale photo-identification is an essential part of the whale physiology toolkit

By Alejandro Fernandez Ajo, PhD student at the Department of Biology, Northern Arizona University, Visiting scientist in the GEMM Lab working on the gray whale physiology and ecology project  

Two years ago, in August 2018, I came to Newport and visited the Hatfield Marine Science Center for the first time with an NSF/RCN-founded laboratory exchange with the GEMM Lab and met Dr. Leigh Torres. My goals during this exchange where to learn about non-invasive fieldwork techniques for studying free-range whales while interacting, exchanging ideas, and networking with the GEMM Lab members; also, to discuss some projects and thoughts for future collaborations with Dr. Torres. During those two weeks in Newport, I had the opportunity to help with field work on the project “Evaluation of gray whale ecology and physiology in response to variable ambient ocean noise conditions”, which aims to evaluate the hormonal variability and health of the gray whales that forage along the Oregon coast in the context of multiple stressors. I would return during the summers of 2019 and 2020 as a visiting scientist and research assistant to work on this project. This year the experience has been a bit different in terms of interactions with the HMSC community due to COVID-19; however, we were able to successfully start the field season in time and now we are wrapping up our second month of surveys with many new and interesting data gathered, and many new, unforgettable memories to be treasured. Working with these animals is incredibly fascinating because there are so many things we don´t know about them, and the questions can become both overwhelming and exciting.

An essential part of this project, and arguably any research project done with cetaceans, is the identification of individuals. Hence, considerable effort is expended each year attempting to photograph every gray whale possible within our study region and to identify each whale we encounter. The GEMM Lab maintains a catalog of the gray whales that visit the Oregon coast, a sub-population known as the Pacific Coast Feeding Group (PCFG). This catalog currently consists of 173 individuals. which we frequently compare with a larger catalog of gray whales that includes 2060 individuals observed since 1977 (Cascadia Research Collective). These methods allow us to know who is who among the whales we encounter each day at sea.

The different species of cetaceans can be individually identified by markings on their bodies, very much like fingerprints in humans. Some features on these animals are unique and conserved through life. For example, Southern and Northern right whales are identified by the callosity patters in their heads (Picture 1), while humpback whales are mostly identified individually by the shape and the patterns of black and white pigmentation on the underside of their fluke (Picture 2). Gray whales have very mottled skin coloration, so we use a combination of markings and features to identify individuals: pigmentation patterns, scars, shape and pigmentation of their fluke, and sometimes the shape of their knuckles, which are a series of “humps” that gray whales have instead of a dorsal fin on their back. It might sound very difficult to do, and it can be a tedious task, however as you train your eye it becomes easier, and features that at first seemed undistinguishable become recognizable and unique (Picture 3). As a reward, it is such a joy to find a match and recognize old friends when they arrive from their long journeys in the vast ocean each year to the Oregon coast.

The callosity pattern of a southern right whale. Photo by Alejandro Fernández Ajó – Instituto de Conservación de Ballenas.
Three different humpback whales with notably different pigmentation patterns on their flukes. Photographs captured under NOAA/NMFS permit #21678.
The gray whale “Knife” we have observed frequently this summer off the Oregon coast. Can you see how the right pigmentation pattern identified looks like a knife? Photograph captured under NOAA/NMFS permit #21678.

As a result of our photo-identification efforts and the high site-fidelity of the whales we study, the large majority of the gray whales we observe here in Oregon are known individually. For many whales, we also have detailed sightings records that can span years and decades, that document calving history, lactation, appearance of scars indicative of injury or entanglement, minimum age, sex, habitat-use patterns, behaviors, etc. Holding such detailed information of individual whales provides incredible contributions to our understanding of the basic patterns in life history of whales, such as reproduction rates, calving intervals, age of first reproduction, etc. Moreover, when these life history events are linked with physiological sample collection large steps can be made in the development and validation of physiological methods. Many endocrine assays currently in use for whales are based on non-traditional sample types including feces, respiratory vapor, and baleen, which have been validated using the catalogs of well-known individuals to verify that measured hormones reflect patterns expected for various physiological states. For example, we can compare endocrine data of confirmed pregnant females, known mature males, and known-injured whales to learn how whale physiological responses are different during different life history events (e.g., Burgess et al. 2017, 2018, Corkeron et al. 2017, Hunt et al. 2006, 2016, 2018, Lysiak et al. 2018, Rolland et al. 2005).

Here in Oregon we are learning from the lives of the gray whales we study, and here I want to share with you two of their stories, one happy and one not-so-happy.

Let´s start with the not-so-happy story so we can end with some brighter news. On June 24 this year, we encountered a whale near Cape Foulweather, which is a very tricky area to work as there are many rocks and shallow water that make the sea conditions very choppy even with low swell. We started documenting the sighting as usual, taking pictures of the left side, the right side and ideally also the fluke of the whale. As we approached this whale, we started noting that something was wrong with its fluke. With the challenging sea conditions, it was not easy to approach the whale and the whale was not exposing its fluke when diving. When we put our drone up to collect photogrammetry and behavior data we gained a much better perspective. This whale has a bad injury on it fluke (Picture 4.C). On the boat we started making conjectures about the cause of this terrible injury that had basically amputate most of its left fluke lobe. Once back on shore, we sorted out the photos and compared the field images captured during the day with the photo-ID catalog and we made a match. This whale is known in our catalog as “ROLLER SKATE”, is a female, and was first sighted in 2015, so she is at least 5 years old today.

The story unfolded when we reviewed Roller Skate’s sighting history. Interestingly we observed this same whale in the same location last September 2019. Unfortunately, it was a very brief encounter but enough for photo documentation of the whale and an interesting observation. Here I quote the field notes that Dr. Torres wrote from this sighting: “September 6th, 2019. Sighting 9: Scattered whales feeding and/or traveling across area to north of Cape Foulweather. One whale had recently chopped fluke; tried to re-find to get better photos but could not (looking at photos now, this whale is clearly entangled in line!). Ceiling too low for UAS [drone flight].” (Picture 4.B).

Progressive photos of Roller Skate’s fluke. In 2017, her fluke was healthy (A). In 2019, we observed her fluke with a line entanglement and “chewed up” (B). In 2020, we have observed the resulting wound and healing process (C). Photographs captured under NOAA/NMFS permit #21678.

Roller skate’s story is an example of how essential is to keep an ID catalog. After a close-up examination of the 2019 picture, we can clearly see a rope entanglement (Picture 4.B). Photos from previous years show how beautiful and healthy her fluke was before this event (Picture 4.A). This event is heart breaking to witness, but this whale could be considered lucky because she was able to shed the gear and survive this entanglement, at least in the short term. Additionally, we can learn from Roller Skate’s misfortune to help us understand what the consequences of such an injury (stressor) may be on the physiology of a whale. We have been eager to collect a fecal sample from Roller Skate to analyze how her hormone levels compare to non-injured whales. Fortunately, we got lucky a couple weeks ago and collected this sample, so now we need to get in the lab and analyze the samples. But more questions remain: Will this injury impact her ability to reproduce? If so, for how long? And at a larger scale, what are the population consequences of such events? If we can understand the magnitude of lethal and sublethal human caused impacts on individual whales and their populations from events such as entanglements, we can develop better methods to mitigate and limit such hazards for whales in their environments.

As I promised, there is also some good news to share. A very well-known PCFG whale, almost a celebrity I dear to say, is “Scarback”, or as we like to call her “Scarlett”. Scarlett is a female known since 1996, making her at least 24 years old, and she also has a very bad injury of unknown origin. Scarlett has a terrible scar on her back that is theorized to have been caused by an explosive harpoon, or maybe a bad ship-strike (Picture 5), but we really do not know. However, we do know she survived this injury and this year she brought a new calf into the population (Picture 6). This is the second calf we have documented from Scarlett, with her previous calf sighted during the 2016 field season and we call it “Brown”. Scarlett is an example of how resilient these amazing giants can be; however, it is likely that while she was recovering from this injury, she was unable to reproduce. How many calves from Scarlett did the PCFG population “lose” due to such a tragedy? We can´t know, but we are learning, and her story will also help us understand whale physiology as we will analyze her fecal hormones and body condition during pregnancy, lactation, and resting phases.

The scar on Scarlett’s back. This significant wound has an unknown origin. Photograph captured under NOAA/NMFS permit #21678.

Scarlett is a survivor. We need to recognize that we are sharing the ocean with different forms of life. We need to acknowledge their existence and understand how our use of the oceans is affecting them, and, more importantly, work toward improving their conditions. I hope that with our research we highlight and communicate how amazing are these animals, and how important are they for marine ecosystems. And ultimately, I hope our work helps minimize the impacts that affect other forms of ocean life that coexist with us, both above and below the surface.

The well-known gray whale “Scarlett” surfaces under her calf while it checks out the GEMM Lab field team. Photo by Alejandro Fernandez Ajo taken under NOAA/NMFS permit #21678.

References:

Burgess, E., Hunt, K. E., Kraus, S. D. and Rolland, R. M. (2016). Get the most out of blow hormones: validation of sampling materials, field storage and extraction techniques for whale respiratory vapor samples. Conservation Physiology, 4, cow024.

Burgess, E. A., Hunt, K. E., Kraus, S. D. and Rolland, R. M. (2018). Quantifying hormones in exhaled breath for physiological assessment of large whales at sea. Scientific Reports, 8, 10031.

Corkeron, P. J., Rolland, R. M., Hunt, K. E. and Kraus, S. D. (2017). A right whale PooTree: Fecal hormones and classification trees identify reproductive states in North Atlantic right whales (Eubalaena glacialis). Conservation Physiology, 5, cox006. DOI: 10.1093/conphys/cox006.

Hunt, K., Lysiak, N., Moore, M. and Rolland, R. (2017). Multi-year longitudinal profiles of cortisol and corticosterone recovered from baleen of North Atlantic right whales (Eubalaena glacialis). General and Comparative Endocrinology, 254, 50-59. DOI: 10.1016/j.ygcen.2017.09.009.

Hunt, K., Lysiak, N. S. J., Matthews, C. J. D., et al. (2018). Multi-year patterns in testosterone, cortisol and corticosterone in baleen from adult males of three whale species. Conservation Physiology, 6, coy049. DOI: 10.1093/conphys/coy049.

Hunt, K. E., Rolland, R. M., Kraus, S. D. and Wasser, S. K. (2006). Analysis of fecal glucocorticoids in the North Atlantic Right Whale (Eubalaena glacialis). General and Comparative Endocrinology, 148, 260-272.

Lysiak, N., Trumble, S., Knowlton, A. and Moore, M. (2018). Characterizing the duration and severity of fishing gear entanglement on a North Atlantic right whale (Eubalaena glacialis) using stable isotopes, steroid and thyroid hormones in baleen. Frontiers in Marine Science. DOI: 10.3389/fmars.2018.00168.

Rolland, R. M., Hunt, K. E., Kraus, S. D. and Wasser, S. K. (2005). Assessing reproductive status of right whales (Eubalaena glacialis) using fecal hormone metabolites. General and Comparative Endocrinology, 142, 308-317.

Whales are amazing, and also provide amazing benefits to our oceans and human society

By Alejandro Fernandez Ajo, PhD student at the Department of Biology, Northern Arizona University, Visiting scientist in the GEMM Lab working on the gray whale physiology and ecology project  

Whales are among the most amazing and enigmatic animals in the world. Whales are not only fascinating, they are also biologically special. Due to their key ecological role and unique biological traits (i.e., their large body size, long lifespans, and sizable home ranges), whales are extremely important in helping sustain the entire marine ecosystem.

Working towards the conservation of marine megafauna, and large charismatic animals in general, is often seen as a mere benevolent effort that conservationist groups, individuals, and governments do on behalf of the individual species. However, mounting evidence demonstrates that restoring populations of marine megafauna, including large whales, can help buffer marine ecosystems from destabilizing stresses like human driven CO2 emissions and global change due to their ability to sequester carbon in their bodies (Pershing et al. 2010). Furthermore, whales can enhance primary production in the ocean through their high consumption and defecation rates, which ultimately provides nutrients to the ecosystem and improves fishery yields (Roman-McCarthy, 2010; Morissette et al. 2012).

Relationships between humans and whales have a long history, however, these relationships have changed. For centuries, whales were valued in terms of the number of oil barrels they could yield, and the quality of their baleen and meat. In the North Atlantic, whaling started as early as 1000 AD with “shore whaling” of North Atlantic right whales by Basque whalers. This whaling was initially limited to the mother and calve pairs that were easy to target due to their coastal habits and the fact that calves are more vulnerable and slower (Reeves-Smith, 2006). Once the calving populations of near-shore waters off Europe were depleted, offshore whaling began developing. Whalers of multiple nations (including USA, British, French, Norwegian, Portuguese, and Dutch, among others), targeted whales around the world, mainly impacting the gray whale populations, and all three right whale species along with the related bowhead whale. Later, throughout the phase of modern whaling using industrialized methods, the main target species consisted of the blue, fin, humpback, minke, sei and sperm whale (Schneider- Pearce, 2004).

By the early twentieth century, many of the world´s whale populations where reduced to a small fraction of their historical numbers, and although pre-whaling abundance of whale stocks is a subject of debate, recent studies estimate that at least the 66%, and perhaps as high as 90% for some whale species and populations (Branch-Williams 2006; Christensen, 2006), where taken during this period. This systematic and serial depletion of whale papulations reduced the biomass and abundance of great whales around the world, which has likely altered the structure and function of the oceans (Balance et al. 2006; Roman et al. 2014; Croll, et al. 2006).

After centuries of unregulated whale hunting, commercial whaling was banned in the mid-twentieth century. This ban was the result of multiple factors including reduced whale stocks below the point where commercial whaling would be profitable, and a fortunate shift in public perception of whales and the emergence of conservation initiatives (Schneider- Pearce, 2004). Since this moratorium on whaling, several whale populations have recovered around the world, and some populations that were listed as endangered have been delisted (i.e., the Eastern North Pacific gray whale) and some populations are estimated to have re-bounced to their pre-whaling abundance.

Although, the recovery of some populations has motivate some communities or nations to obtain or extend their whaling quotas (see Blog Post by Lisa Hildebrand), it is important to acknowledge that the management of whale populations is arguably one of the most complicated tasks, and is distinguished from management of normal fisheries due to various biological aspects. Whales are long living mammals with slow reproduction rates, and on average a whale can only produce a calf every two or three years. Hence, the gross addition to the stock rarely would exceed 25% of the number of adults (Schneider- Pearce, 2004), which is a much lower recovery rate that any fish stock. Also, whales usually reach their age of sexual maturity at 6-10 years old, and for many species there are several uncertainties about their biology and natural history that make estimations of population abundance and growth rate even harder to estimate.

Fig 1: Human relationship with whales has changed through history. Once valued for their meat and oil, now they are a natural attraction that amaze and attract crowds to whale watching destinations all over the globe. Photo: Stephen Johnson, Península Valdés-Argentina.

Moreover, while today´s whales are generally not killed directly by hunting, they are exposed to a variety of other increasing human stressors (e.g., entanglement in fishing gear, vessel strikes, shipping noise, and climate change). Thus, scientists must develop novel tools to overcome the challenges of studying whales and distinguish the relative importance of the different impacts to help guide conservation actions that improve the recovery and restoration of whale stocks (Hunt et al. in press). With the restoration of great whale populations, we can expect positive changes in the structure and function of the world’s oceans (Chami et al. 2019; Roman et al. 2010).

So, why it is worth keeping whales healthy?

Whales facilitate the transfer of nutrients by (1) releasing nutrient-rich fecal plumes near the surface after they have feed at depth and (2) by moving nutrients from highly productive, polar and subpolar latitude feeding areas to the low latitude calving areas (Roman et al. 2010). In this way, whales help increase the productivity of phytoplankton that in turn support zooplankton production, and thus have a bottom up effect on the productivity of many species including fish, birds, and marine mammals, including whales. These fertilization events can also facilitate mitigation of the negative impacts of climate change. The amount of iron contained in the whales’ feces can be 10 million times greater than the level of iron in the marine environment, triggering important phytoplankton blooms, which in turn sequester thousands of tons of carbon from, and release oxygen to, the atmosphere annually (Roman et al. 2016; Smith et al. 2013; Willis, 2007). Furthermore, when whales die, their massive bodies fall to the seafloor, making them the largest and most nutritious source of food waste, which is capable of sustaining a succession of macro-fauna assemblages for several decades, including some invertebrate species that are endemic to whale carcasses (Smith et al. 2015).

Figure 2. The figure shows a conceptual model of the “whale pump”. From Roman-McCarthy, 2010.

Despite the several environmental services that whales provide, and the positive impact on local economies that depend on whale watching tourism, which has been valued in millions of dollars per year (Hoyt E., 2001), the return of whales and other marine mammals has often been implicated in declines in fish populations, resulting in conflicts with human fisheries (Lavigne, D.M. 2003). Yet there is insufficient direct evidence for such competition (Morissette et al. 2010). Indeed, there is evidence of the contrary: In ecosystem models where whale abundances are reduced, fish stocks show significant decreases, and in some cases the presence of whales in these models result in improved fishery yields. Consistent with these findings, several models have shown that alterations in marine ecosystems resulting from the removal of whales and other marine mammals do not lead to increases in human fishery yields (Morissette et al. 2010; 2012). Although the environmental services and benefits provided by great whales, which potentially includes the enhancement of fisheries yields, and enhancement on ocean oxygen production and capturing carbon, are evident and make a strong argument for improved whale conservation, it is overwhelming how little we know about many aspects of their lives, their biology, and particularly their physiology.

Figure 3: Whales are the most fascinating animals in the world, but they are not only amazing animals. They are also extremely important in sustaining the entire marine ecosystem. Photo: Alejandro Fernández Ajó -Instituto de Conservación de ballenas.

This lack of knowledge is because whales are really hard to study. For many years research was limited to the observation of the brief surfacing of the whales, yet most of their lives occurs beneath the surface and were completely unknown. Fortunately, new technologies and the creativity of whale researchers are helping us to better understand many aspects of their lives that were cryptic to us even a decade ago. I am committed to filling some of these knowledge gaps. My research examines how different environmental and anthropogenic impacts affect whale health, and particularly how these impacts may relate to cases of large whale mortalities and declines in whale populations. I am applying novel methods in conservation physiology for measuring hormone levels that promise to improve our understanding of the relationship between different (extrinsic and intrinsic) stressors and the physiological response of whales. Ultimately, this research will help address important conservation questions, such as the causes of unusual whale mortality events and declines in whale populations.

References:

Ballance LT, Pitman RL, Hewitt R, et al. 2006. The removal of large whales from the Southern Ocean: evidence for long-term ecosystem effects. In: Estes JA, DeMaster DP, Doak DF, et al. (Eds). Whales, whaling and ocean ecosystems. Berkeley, CA: University of California Press.

Branch TA and Williams TM. 2006. Legacy of industrial whaling. In: Estes JA, DeMaster DP, Doak DF, et al. (Eds). Whales, whaling and ocean ecosystems. Berkeley, CA: University of California Press.

Chami, R. Cosimano, T. Fullenkamp, C. & Oztosun, S. (2019). Nature’s solution to climate change. Finance & Development, 56(4).

Christensen LB. 2006. Marine mammal populations: reconstructing historical abundances at the global scale. Vancouver, Canada: University of British Columbia.

Croll DA, Kudela R, Tershy BR (2006) Ecosystem impact of the decline of large whales in the North Pacific. In: Estes JA, DeMaster DP, Doak DF, Williams TM, BrownellJr RL, editors. Whales, Whaling, and Ocean Ecosystems. Berkeley: University of California Press. pp. 202–214.

Hoyt, E. 2001. Whale Watching 2001: Worldwide Tourism Numbers, Expenditures and Expanding Socioeconomic Benefits

Hunt, K.E., Fernández Ajó, A. Lowe, C. Burgess, E.A. Buck, C.L. In press. A tale of two whales: putting physiological tools to work for North Atlantic and southern right whales. In: “Conservation Physiology: Integrating Physiology Into Animal Conservation And Management”, ch. 12. Eds. Madliger CL, Franklin CE, Love OP, Cooke SJ. Oxford University press: Oxford, UK.

Lavigne, D.M. 2003. Marine mammals and fisheries: the role of science in the culling debate. In: Gales N, Hindell M, and Kirkwood R (Eds). Marine mammals: fisheries, tourism, and management issues. Melbourne, Australia: CSIRO.

Morissette L, Christensen V, and Pauly D. 2012. Marine mammal impacts in exploited ecosystems: would large scale culling benefit fisheries? PLoS ONE 7: e43966.

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

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

Reeves, R. and Smith, T. (2006). A taxonomy of world whaling. In DeMaster, D. P., Doak, D. F., Williams, T. M., and Brownell Jr., R. L., eds. Whales, Whaling, and Ocean Ecosystems. University of California Press, Berkeley, CA.

Roman, J. Altman I, Dunphy-Daly MM, et al. 2013. The Marine Mammal Protection Act at 40: status, recovery, and future of US marine mammals. Ann NY Acad Sci; doi:10.1111/nyas.12040.

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

Roman, J. Estes, J.A. Morissette, L. Smith, C. Costa, D. McCarthy, J. Nation, J.B. Nicol, S. Pershing, A.and Smetacek, V. 2014. Whales as marine ecosystem engineers. Frontiers in Ecology and the Environment. 12(7). 377-385.

Roman, J. Nevins, J. Altabet, M. Koopman, H. and McCarthy, J. 2016. Endangered right whales enhance primary productivity in the Bay of Fundy. PLoS ONE. 11(6): e0156553.

Schneider, V. Pearce, D. What saved the whales? An economic analysis of 20th century whaling. Biodiversity and Conservation 13, 543–562 (2004). https://doi org.libproxy.nau.edu/10.1023/B:BIOC.0000009489.08502.1

Smith LV, McMinn A, Martin A, et al. 2013. Preliminary investigation into the stimulation of phyto- plankton photophysiology and growth by whale faeces. J Exp Mar Biol Ecol 446: 1–9.

Smith, C.R. Glover, A.G. Treude, T. Higgs, N.D. and Amon, D.J. 2015. Whale-fall ecosystems: Recent insights into ecology, paleoecology, and evolution. Annu. Rev. Marine. Sci. 7:571-596.

Willis, J. 2007. Could whales have maintained a high abundance of krill? Evol Ecol Res 9: 651–662.

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.

The significance of blubber hormone sampling in conservation and monitoring of marine mammals

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

Marine mammals are challenging to study for many reasons, and specifically because they inhabit the areas of the Earth that are uninhabited by people: the oceans. Monitoring marine mammal populations to gather baselines on their health condition and reproductive status is not as simple as trap and release, which is a method often conducted for terrestrial animals. Marine mammals are constantly moving in vast areas below the surface. Moreover, cetaceans, which do not spend time on land, are arguably the most challenging to sample.

One component of my project, based in California, USA, is a health assessment analyzing hormones of the bottlenose dolphins that frequent both the coastal and the offshore waters. Therefore, I am all too familiar with the hurdles of collecting health data from living marine mammals, especially cetaceans. However, the past few decades have seen major advancements in technology both in the laboratory and with equipment, including one tool that continues to be critical in understanding cetacean health: blubber biopsies.

Biopsy dart hitting a bottlenose dolphin below the dorsal fin. Image Source: NMFS

Blubber biopsies are typically obtained via low-powered crossbow with a bumper affixed to the arrow to de-power it once it hits the skin. The arrow tip has a small, pronged metal attachment to collect an eraser-tipped size amount of tissue with surface blubber and skin. I compare this to a skin punch biopsies in humans; it’s small, minimally-invasive, and requires no follow-up care. With a small team of scientists, we use small, rigid-inflatable vessels to survey the known locations of where the bottlenose dolphins tend to gather. Then, we assess the conditions of the seas and of the animals, first making sure we are collecting from animals without potentially lowered immune systems (no large, visible wounds) or calves (less than one years old). Once we have photographed the individual’s dorsal fin to identify the individual, one person assembles the biopsy dart and crossbow apparatus following sterile procedures when attaching the biopsy tips to avoid infection. Another person prepares to photograph the animal to match the biopsy information to the individual dolphin. One scientist aims the crossbow for the body of the dolphin, directly below the dorsal fin, while the another photographs the biopsy dart hitting the animal and watches where it bounces off. Then, the boat maneuvers to the floating biopsy dart to recover the dart and the sample. Finally, the tip with blubber and skin tissue is collected, again using sterile procedures, and the sample is archived for further processing. A similar process, using an air gun instead of a crossbow can be viewed below:

GEMM Lab members using an air gun loaded with a biopsy dart to procure marine mammal blubber from a blue whale in New Zealand. Video Source: GEMM Laboratory.

Part of the biopsy process is holding ourselves to the highest standards in our minimally-invasive technique, which requires constant practice, even on land.

Alexa practicing proper crossbow technique on land under supervision. Image Source: Alexa Kownacki

Blubber is the lipid-rich, vascularized tissue under the epidermis that is used in thermoregulation and fat storage for marine mammals. Blubber is an ideal matrix for storing lipophilic (fat-loving) steroid hormones because of its high fat content. Steroid hormones, such as cortisol, progesterone, and testosterone, are naturally circulating in the blood stream and are released in high concentrations during specific events. Unlike blood, blubber is less dynamic and therefore tells a much longer history of the animal’s nutritional state, environmental exposure, stress level, and life history status. Blubber is the cribs-notes version of a marine mammal’s biography over its previous few months of life. Blood, on the other hand, is the news story from the last 24 hours. Both matrices serve a specific purpose in telling the story, but blubber is much more feasible to obtain from a cetacean and provides a longer time frame in terms of information on the past.

A simplified depiction of marine mammal blubber starting from the top (most exterior surface) being the skin surface down to the muscle (most interior). Image Source: schoolnet.org.za

I use blubber biopsies for assessing cortisol, testosterone, and progesterone in the bottlenose dolphins. Cortisol is a glucocorticoid that is frequently associated with stress, including in humans. Marine mammals utilize the same hypothalamic-pituitary-adrenal (HPA) axis that is responsible for the fight-or-flight response, as well as other metabolic regulations. During prolonged stressful events, cortisol levels will remain elevated, which has long-term repercussions for an animal’s health, such as lowered immune systems and decreased ability to respond to predators. Testosterone and progesterone are sex hormones, which can be used to indicate sex of the individual and determine reproductive status. This reproductive information allows us to assess the population’s composition and structure of males and females, as well as potential growth or decline in population (West et al. 2014).

Alexa using a crossbow from a small boat off of San Diego, CA. Image Source: Alexa Kownacki

The coastal and offshore bottlenose dolphin ecotypes of interest in my research occupy different locations and are therefore exposed to different health threats. This is a primary reason for conducting health assessments, specifically analyzing blubber hormone levels. The offshore ecotype is found many kilometers offshore and is most often encountered around the southern Channel Islands. In contrast, the coastal ecotype is found within 2 kilometers of shore (Lowther-Thieleking et al. 2015) where they are subjected to more human exposure, both directly and indirectly, because of their close proximity to the mainland of the United States. Coastal dolphins have a higher likelihood of fishery-related mortality, the negative effects of urbanization including coastal runoff and habitat degradation, and recreational activities (Hwang et al. 2014). The blubber hormone data from my project will inform which demographics are most at-risk. From this information, I can provide data supporting why specific resources should be allocated differently and therefore help vulnerable populations. Further proving that the small amount of tissue from a blubber biopsy can help secure a better future for population by adjusting and informing conservation strategies.

Literature Cited:

Hwang, Alice, Richard H Defran, Maddalena Bearzi, Daniela. Maldini, Charles A Saylan, Aime ́e R Lang, Kimberly J Dudzik, Oscar R Guzo n-Zatarain, Dennis L Kelly, and David W Weller. 2014. “Coastal Range and Movements of Common Bottlenose Dolphins (Tursiops Truncatus) off California and Baja California, Mexico.” Bulletin of the Southern California Academy of Sciences 113 (1): 1–13. https://doi.org/10.3390/toxins6010211.

Lowther-Thieleking, Janet L., Frederick I. Archer, Aimee R. Lang, and David W. Weller. 2015. “Genetic Differentiation among Coastal and Offshore Common Bottlenose Dolphins, Tursiops Truncatus, in the Eastern North Pacific Ocean.” Marine Mammal Science 31 (1): 1–20. https://doi.org/10.1111/mms.12135.

West, Kristi L., Jan Ramer, Janine L. Brown, Jay Sweeney, Erin M. Hanahoe, Tom Reidarson, Jeffry Proudfoot, and Don R. Bergfelt. 2014. “Thyroid Hormone Concentrations in Relation to Age, Sex, Pregnancy, and Perinatal Loss in Bottlenose Dolphins (Tursiops Truncatus).” General and Comparative Endocrinology 197: 73–81. https://doi.org/10.1016/j.ygcen.2013.11.021.

Applying novel methods in conservation physiology to understand cases of large whale mortalities

By Alejandro Fernánez Ajó, PhD student at NAU and GEMM Lab research technician

Although commercial whaling is currently banned and several whale populations show evidence of recovery, today´s whales are exposed to a variety of other human stressors (e.g., entanglement in fishing gear, vessel strikes, shipping noise, climate change, etc.; reviewed in Hunt et al., 2017a). The recovery and conservation of large whale populations is particularly important to the oceanic environment due to their key ecological role and unique biological traits, including their large body size, long lifespan and sizable home ranges (Magera et al., 2013; Atkinson et al., 2015; Thomas and Reeves, 2015). Thus, scientists must develop novel tools to overcome the challenges of studying whale physiology in order to distinguish the relative importance of the different impacts and guide conservation actions accordingly (Ayres et al., 2012; Hunt et al., 2013).

To this end, baleen hormone analysis represents a powerful tool for retrospective assessment of patterns in whale physiology (Hunt et al., 2014, 2016, 2017a, 2017b, 2018; Lysiak et. al., 2018; Fernández Ajó et al., 2018; Rolland et al., 2019). Moreover, hormonal panels, which include multiple hormones, are helping to better clarify and distinguish between the physiological effects of different sources of anthropogenic and environmental stressors (Ayres et al., 2012; Wasser et al., 2017; Lysiak et al., 2018; Romero et al., 2015).

What is Baleen? Baleen is a stratified epithelial tissue consisting of long, fringed plates that grow downward from the upper jaw, which collectively form the whale´s filter-feeding apparatus (Figure 1). This tissue accumulates hormones as it grows. Hormones are deposited in a linear fashion with time so that a single plate of baleen allows retrospective assessment and evaluation of a whales’ physiological condition, and in calves baleen provides a record of the entire lifespan including part of their gestation. Baleen samples are also readily accessible and routinely collected during necropsy along with other samples and relevant information.

Figure 1: Top: A baleen plate from a southern right whale calf (Source: Fernández Ajó et al. 2018). Bottom: A southern right whale with mouth open exposing its baleen (photo credit: Stephen Johnson).

Why are the Southern Right Whales calves (SRW) dying in Patagonia?

I am a Fulbright Ph.D. student in the Buck Laboratory  at Northern Arizona University since Fall 2017, a researcher with the Whale Conservation Institute of Argentina (Instituto de Conservación de Ballenas) and Field Technician for the GEMM Lab over the summer. I focus my research on the application and development of novel methods in conservation physiology to improve our understanding of how physiological parameters are affected by human pressures that impact large whales and marine mammals. I am especially interested in understanding the underlaying causes of large whale mortalities with the aim of preventing their occurrence when possible. In particular, for my Ph.D. dissertation, I am studying a die-off case of Southern Right Whale (SRW) calves, Eubalaena australis, off Peninsula Valdés (PV) in Patagonia-Argentina (Figure 2).

Prior to 2000, annual calf mortality at PV was considered normal and tracked the population growth rate (Rowntree et al., 2013). However, between 2007 and 2013, 558 whales died, including 513 newborn calves (Sironi et al., 2018). Average total whale deaths per year increased tenfold, from 8.2 in 1993-2002 to 80 in 2007-2013. These mortality levels have never before been observed for the species or any other population of whales (Thomas et al., 2013, Sironi et al., 2018).


Figure 2: Study area, the red dots along the shoreline indicate the location where the whales were found stranded at Península Valdés in 2018 (Source: The Right Whale Program Research Report 2018, Sironi and Rowntree, 2018)

Among several hypotheses proposed to explain these elevated calf mortalities, harassment by Kelp Gulls, Larus dominicanus, on young calves stands out as a plausible cause and is a unique problem only seen at the PV calving ground. Kelp gull parasitism on SRWs near PV was first observed in the 1970’s (Thomas, 1988). Gulls primarily harass mother-calf pairs, and this parasitic behavior includes pecking on the backs of the whales and creating open wounds to feed on their skin and blubber. The current intensity of gull harassment has been identified as a significant environmental stressor to whales and potential contributor to calf deaths (Marón et al., 2015b; Fernández Ajó et al., 2018).

Figure 3: The significant preference for calves as a target of gull attacks highlights the impact of this parasitic behavior on this age class. The situation continues to be worrisome and serious for the health and well-being of newborn calves at Península Valdés. Left: A Kelp Gull landing on whale´s back to feed on her skin and blubber (Photo credit: Lisandro Crespo). Right: A calf with multiple lesions on its back produced by repeated gull attacks (Photo credit: ICB).

Quantifying gull inflicted wounds

Photographs of gull wounds on whales taken during necropsies and were quantified and assigned to one of seven objectively defined size categories (Fig. 4): extra-small (XS), small (S), medium (M), large (L), extra-large (XL), double XL (XXL) and triple XL (XXXL). The size and number of lesions on each whale were compared to baleen hormones to determine the effect of the of the attacks on the whales health.

Figure 4. Kelp gull lesion scoring. Source: Maron et al. 2015).

How baleen hormones are applied

Impact factors such as injuries, predation avoidance, storms, and starvation promote an increase in the secretion of the glucocorticoids (GCs) cortisol and corticosterone (stress hormones), which then induce a variety of physiological and behavioral responses that help animals cope with the stressor. Prolonged exposure to chronic stress, however, may exceed the animal’s ability to cope with such stimuli and, therefore, adversely affects its body condition, its health, and even its survival. Triiodothyronine (T3), is the most biologically active form of the thyroid hormones and helps regulate metabolism. Sustained food deprivation causes a decrease in T3 concentrations, slowing metabolism to conserve energy stores. Combining GCs and T3 hormone measures allowed us to investigate and distinguish the relative impacts of nutritional and other sources of stressors.

Combining these novel methods produced unique results about whale physiology. With my research, we are finding that the GCs concentrations measured in calves´ baleen positively correlate with the intensity of gull wounding (Figure 4, 1 and 2), while calf’s baleen thyroid hormone concentrations are relative stable across time and do not correlate with intensity of gull wounding (Figure 4 – 3). Taken together these findings indicate that SRW calves exposed to Kelp gull parasitism and harassment experience high levels of physiological stress that compromise their health and survival. Ultimately these results will inform government officials and managers to direct conservation actions aimed to reduce the negative interaction between Kelp gulls and Southern Right Whales in Patagonia.

Figure 4: Physiological stress correlates with number of gull lesions (1 and 2). According to the best-fit linear model, immunoreactive baleen corticosterone (B) and cortisol (F) concentrations increased with wound severity (i.e. number of gull lesions). However, nutritional status indexed by baleen immunoreactive triiodothyronine (T3) concentrations does not correlate with the number of gull lesions (3). (Fernández Ajó et al. 2019, manuscript under revision)

Baleen hormones as a conservation tool

Baleen hormones represent a powerful tool for retrospective assessments of longitudinal trends in whale physiology by helping discriminate the underlying mechanisms by which different stressors may affect a whale’s health and physiology. Moreover, while most sample types used for studying whale physiology provide single time-point measures of current circulating hormone levels (e.g., skin or respiratory vapor), or information from previous few hours or days (e.g., urine and feces), baleen tissue provides a unique opportunity for longitudinal analyses of hormone patterns. These retrospective analyses can be conducted for both stranded or archived specimens, and can be conducted jointly with other biological markers (e.g., stable isotopes and biotoxins) to describe migration patterns and exposure to pollutants. Further research efforts on baleen hormones should focus on completing biological validations to better understand the hormone measurements in baleen and its correlation with measurements from alternative sample matrices (i.e., feces, skin, blubber, and respiratory vapors).

References:

Atkinson, S., Crocker, D., Houser, D., Mashburn, K., 2015. Stress physiology in marine mammals: how well do they fit the terrestrial model? J. Comp. Physiol. B. 185, 463–486. https://doi.org/10.1007/s00360-015-0901-0.

Ayres, K.L., Booth, R.K., Hempelmann, J.A., Koski, K.L., Emmons, C.K., Baird, R.W., Balcomb-Bartok, K., Hanson, M.B., Ford, M.J., Wasser, S.K., 2012. Distinguishing the impacts of inadequate prey and vessel traffic on an endangered killer whale (Orcinus orca) population. PLoS ONE. 7, e36842. https://doi.org/10.1371/journal.pone.0036842.

Fernández Ajó, A.A., Hunt, K., Uhart, M., Rowntree, V., Sironi, M., Marón, C.F., Di Martino, M., Buck, L., 2018. Lifetime glucocorticoid profiles in baleen of right whale calves: potential relationships to chronic stress of repeated wounding by Kelp Gull. Conserv. Physiol. 6, coy045. https://doi.org/10.1093/conphys/coy045.

Hunt, K., Lysiak, N., Moore, M., Rolland, R.M., 2017a. Multi-year longitudinal profiles of cortisol and corticosterone recovered from baleen of North Atlantic right whales (Eubalaena glacialis). Gen. Comp. Endocrinol. 254: 50–59. https://doi.org/10.1016/j.ygcen.2017.09.009.

Hunt, K.E., Hunt, K.E., Lysiak, N.S., Matthews, C.J.D., Lowe, C., Fernández-Ajo, A., Dillon, D., Willing, C., Heide-Jørgensen, M.P., Ferguson, S.H., Moore, M.J., Buck, C.L., 2018. Multi-year patterns in testosterone, cortisol and corticosterone in baleen from adult males of three whale species. Conserv. Physiol. 6, coy049. https://doi.org/10.1093/conphys/coy049.

Hunt, K.E., Hunt, K.E., Lysiak, N.S., Moore, M.J., Rolland R.M., 2016. Longitudinal progesterone profiles in baleen from female North Atlantic right whales (Eubalaena glacialis) match known calving history. Conserv. Physiol. 4, cow014. https://doi.org/10.1093/conphys/cow014.

Hunt, K.E., Lysiak, N.S., Moore, M.J., Seton, R.E., Torres, L., Buck, C.L., 2017b. Multiple steroid and thyroid hormones detected in baleen from eight whale species. Conserv. Physiol. 5, cox061. https://doi.org/10.1093/conphys/cox061.

Hunt, K.E., Moore, M.J., Rolland, R.M., Kellar, N.M., Hall, A.J., Kershaw, J., Raverty, S.A., Davis, C.E., Yeates, L.C., Fauquier, D.A., Rowles, T.K., Kraus, S.D., 2013. Overcoming the challenges of studying conservation physiology in large whales: a review of available methods. Conserv. Physiol. 1: cot006. https://doi.org/10.1093/conphys/cot006.

Hunt, K.E., Stimmelmayr, R., George, C., Hanns, C., Suydam, R., Brower, H., Rolland, R.M., 2014. Baleen hormones: a novel tool for retrospective assessment of stress and reproduction in bowhead whales (Balaena mysticetus). Conserv. Physiol. 2, cou030. doi: https://doi.org/10.1093/conphys/cou030.

Lysiak, N., Trumble, S., Knowlton, A., Moore, M., 2018. Characterizing the duration and severity of fishing gear entanglement on a North Atlantic right whale (Eubalaena glacialis) using stable isotopes, steroid and thyroid hormones in baleen. Front. Mar. Sci. 5: 168. https://doi.org/10.3389/fmars.2018.00168.

Magera, A.M., Flemming, J.E.M., Kaschner, K., Christensen, L.B., Lotze, H.K., 2013. Recovery trends in marine mammal populations. PLoS ONE. 8, e77908. https://doi.org/10.1371/journal.pone.0077908.

Marón, C.F., Beltramino, L., Di Martino, M., Chirife, A., Seger, J., Uhart, M., Sironi, M., Rowntree, V.J., 2015b Increased wounding of southern right whale (Eubalaena australis) calves by Kelp Gulls (Larus dominicanus) at Península Valdés, Argentina., PLoS ONE. 10, p. e0139291. https://doi.org/10.1371/journal.pone.0139291.

Marón, C.F., Rowntree, V.J., Sironi, M., Uhart, M., Payne, R.S., Adler, F.R., Seger, J., 2015a. Estimating population consequences of increased calf mortality in the southern right whales off Argentina. SC/66a/BRG/1 presented to the IWC Scientific Committee, San Diego, USA. Available at: https://iwc.int/home

Rolland, R.M., Graham, K.M., Stimmelmayr, R., Suydam, R. S., George, J.C., 2019. Chronic stress from fishing gear entanglement is recorded in baleen from a bowhead whale (Balaena mysticetus). Mar. Mam. Sci. https://doi.org/10.1111/mms.12596.

Romero, L.M., Platts, S.H., Schoech, S.J., Wada, H., Crespi, E., Martin, L.B., Buck, C.L., 2015. Understanding Stress in the Healthy Animal – Potential Paths for Progress. Stress. 18(5), 491-497.

Rowntree, V.J., Uhart, M.M., Sironi, M., Chirife, A., Di Martino, M., La Sala, L., Musmeci, L., Mohamed, N., Andrejuk, J., McAloose, D., Sala, J., Carribero, A., Rally, H., Franco, M., Adler, F., Brownell, R. Jr, Seger, J., Rowles, T., 2013. Unexplained recurring high mortality of southern right whale Eubalaena australis calves at Península Valdés, Argentina. Mar. Ecol. Prog. Ser. 493:275–289. https://doi.org/10.3354/meps10506.

Sironi, M. Rowntree, V., Di Martino, M., Alzugaray, L.,Rago, V., Marón, C.F., Uhart M., 2018. Southern right whale mortalities at Península Valdes, Argentina: updated information for 2016-2017. SC/67B/CMP/06 presented to the IWC Scientific Committee, Slovenia. Available at: https://iwc.int/home.

Sironi, M. Rowntree, V., Snowdon, C., Valenzuela, L., Marón C., 2009. Kelp Gulls (Larus dominicanus) feeding on southern right whales (Eubalaena australis) at Península Valdes, Argentina: updated estimates and conservation implications. SC/61/BRG19. presented to the IWC Scientific Committee, Portugal. Available at: https://iwc.int/home.

Thomas, P., Reeves, R., 2015. Status of the world’s baleen whales. Mar. Mam. Sci. 32:682–734. https://doi.org/10.1111/mms.12281.

Thomas, P., Uhart, M., McAloose, D., Sironi, M., Rowntree, V.J., Brownell, Jr. R., Gulland, F.M.D., Moore, M., Marón, C., Wilson, C., 2013. Workshop on the southern right whale die-off at Península Valdés, Argentina. SC/60/BRG15 presented to the IWC Scientific Committee, South Korea. Available at: https://iwc.int/home

Thomas, P.O. 1988. Kelp Gulls, Larus dominicanus, are parasites on flesh of the right whale, Eubalaena australis. Ethology. 79:89-103. https://doi.org/10.1111/j.1439-0310.1988.tb00703.x.

Wasser, S.K., Lundin, J.I., Ayres, K., Seely, E., Giles, D., Balcomb, K., Hempelmann, J., Parsons, K., Booth, R., 2017. Population growth is limited by nutritional impacts on pregnancy success in endangered Southern Resident killer whales (Orcinus orca). PLoS ONE. 12, e0179824. https://doi.org/10.1371/journal.pone.0179824.

Lingering questions on the potential to bring sea otters back to Oregon

By Dominique Kone, Masters Student in Marine Resource Management

By now, I’m sure you’re aware of recent interests to reintroduce sea otters to Oregon. To inform this effort, my research focuses on predicting suitable sea otter habitat and investigating the potential ecological effects if sea otters are reintroduced in the future. This information will help managers gain a better understanding of the potential for sea otters to reestablish in Oregon, as well as how Oregon’s ecosystems may change via top-down processes. These analyses will address some sources of uncertainties of this effort, but there are still many more questions researchers could address to further guide this process. Here, I note some lingering questions I’ve come across in the course of conducting my research. This is not a complete list of all questions that could or should be investigated, but they represent some of the most interesting questions I have and others have in Oregon.

Credit: Todd Mcleish

The questions, and our associated knowledge on each of these topics:

Is there enough available prey to support a robust sea otter population in Oregon?

Sea otters require approximately 30% of their own body weight in food every day (Costa 1978, Reidman & Estes 1990). With a large appetite, they not only need to spend most of their time foraging, but require a steady supply of prey to survive. For predators, we assume the presence of suitable habitat is a reliable proxy for prey availability (Redfern et al. 2006). Whereby, quality habitat should supply enough prey to sustain predators at higher trophic levels.

In making these habitat predictions for sea otters, we must also recognize the potential limitations of this “habitat equals prey” paradigm, in that there may be parcels of habitat where prey is unavailable or inaccessible. In Oregon, there could be unknown processes unique to our nearshore ecosystems that would support less prey for sea otters. This possibility highlights the importance of not only understanding how much suitable habitat is available for foraging sea otters, but also how much prey is available in these habitats to sustain a viable otter population in the future. Supplementing these habitat predictions with fishery-independent prey surveys is one way to address this question.

Credit: Suzi Eszterhas via Smithsonian Magazine

How will Oregon’s oceanographic seasonality alter or impact habitat suitability?

Sea otters along the California coast exist in an environment with persistent Giant kelp beds, moderate to low wave intensity, and year-round upwelling regimes. These environmental variables and habitat factors create productive ecosystems that provide quality sea otter habitat and a steady supply of prey; thus, supporting high densities of sea otters. This environment contrasts with the Oregon coast, which is characterized by seasonal changes in bull kelp and wave intensity. Summer months have dense kelp beds, calm surf, and strong upwellings. While winter months have little to no kelp, weak upwellings, and intense wave climates. These seasonal variations raise the question as to how these temporal fluctuations in available habitat could impact the number of sea otters able to survive in Oregon.

In Washington – an environment like Oregon – sea otters exhibit seasonal distribution patterns in response to intensifying wave climates. During calm summer months, sea otters primarily forage along the outer coast, but move into more protected areas, such as the Strait of Juan de Fuca, during winter months (Laidre et al. 2009). If sea otters were reintroduced to Oregon, we may very well observe similar seasonal movement patterns (e.g. dispersal into estuaries), but the degree to which this seasonal redistribution and reduction in foraging habitat could impact sea otter reestablishment and recovery is currently unknown.

Credit: Oregon Coast Aquarium

In the event of a reintroduction, do northern or southern sea otters have a greater capacity to adapt to Oregon environments?

In the early 1970’s, Oregon’s first sea otter translocation effort failed (Jameson et al. 1982). Since then, hypotheses on the potential ecological differences between northern and southern sea otters have been proposed as potential factors of the failed effort, potentially due to different abilities to exploit specific prey species. Studies have demonstrated that northern and southern sea otters have slight morphological differences – northern otters having larger skulls and teeth than southern otters (Wilson et al. 1991). This finding has created the hypothesis that the northern otter’s larger skull and teeth allow it to consume prey with denser exoskeletons, and thereby can exploit a greater diversity of prey species. However, there appears to be a lack of evidence to suggest larger skulls and teeth translate to greater bite force. Based on morphology alone, either sub-species could be just as successful in exploiting different prey species.

A different direction to address questions around adaptability is to look at similarities in habitat and oceanographic characteristics. Sea otters exist along a gradient of habitat types (e.g. kelp forests, estuaries, soft-sediment environments) and oceanographic conditions (e.g. warm-temperature to cooler sub-Arctic waters) (Laidre et al. 2009, Lafferty et al. 2014). Yet, we currently don’t know how well or quickly otters can adapt when they expand into new habitats that differ from ones they are familiar with. Sea otters must be efficient foragers and need to acquire skills that allow them to effectively hunt specific prey species (Estes et al. 2003). Hypothetically, if we take sea otters from rocky environments where they’ve developed foraging skills to hunt sea urchins and abalones, and place them in a soft-sediment environment, how quickly would they develop new foraging skills to exploit soft-sediment prey species? Would they adapt quickly enough to meet their daily prey requirements?

Credit: Eric Risberg/Associated Press via The Columbian

In Oregon, specifically, how might climate change impact sea otters, and how might sea otters mediate climate impacts?

Climate change has been shown to directly impact many species via changes in temperature (Chen et al. 2011). Some species have specific thermal tolerances, in which they can only survive within a specified temperature range (i.e. maximum and minimum). Once the temperature moves out of that range, the species can either move with those shifting water masses, behaviorally adapt or perish (Sunday et al. 2012). It’s unclear if and how changing temperatures will impact sea otters, directly. However, sea otters could still be indirectly affected via impacts to their prey. If prey species in sea otter habitat decline due to changing temperatures, this would reduce available food for otters. Ocean acidification (OA) is another climate-induced process that could indirectly impact sea otters. By creating chemical conditions that make it difficult for species to form shells, OA could decrease the availability of some prey species, as well (Gaylord et al. 2011).

Interestingly, these pathways between sea otters and climate change become more complex when we consider the potentially mediating effects from sea otters. Aquatic plants – such as kelp and seagrass – can reduce the impacts of climate change by absorbing and taking carbon out of the water column (Krause-Jensen & Duarte 2016). This carbon sequestration can then decrease acidic conditions from OA and mediate the negative impacts to shell-forming species. When sea otters catalyze a tropic cascade, in which herbivores are reduced and aquatic plants are restored, they could increase rates of carbon sequestration. While sea otters could be an effective tool against climate impacts, it’s not clear how this predator and catalyst will balance each other out. We first need to investigate the potential magnitude – both temporal and spatial – of these two processes to make any predictions about how sea otters and climate change might interact here in Oregon.

Credit: National Wildlife Federation

In Summary

There are several questions I’ve noted here that warrant further investigation and could be a focus for future research as this potential sea otter reintroduction effort progresses. These are by no means every question that should be addressed, but they do represent topics or themes I have come across several times in my own research or in conversations with other researchers and managers. I think it’s also important to recognize that these questions predominantly relate to the natural sciences and reflect my interest as an ecologist. The number of relevant questions that would inform this effort could grow infinitely large if we expand our disciplines to the social sciences, economics, genetics, so on and so forth. Lastly, these questions highlight the important point that there is still a lot we currently don’t know about (1) the ecology and natural behavior of sea otters, and (2) what a future with sea otters in Oregon might look like. As with any new idea, there will always be more questions than concrete answers, but we – here in the GEMM Lab – are working hard to address the most crucial ones first and provide reliable answers and information wherever we can.

References:

Chen, I., Hill, J. K., Ohlemuller, R., Roy, D. B., and C. D. Thomas. 2011. Rapid range shifts of species associated with high levels of climate warming. Science. 333: 1024-1026.

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., Riedman, M. L., Staedler, M. M., Tinker, M. T., and B. E. Lyon. 2003. Individual variation in prey selection by sea otters: patterns, causes and implications. Journal of Animal Ecology. 72: 144-155.

Gaylord et al. 2011. Functional impacts of ocean acidification in an ecologically critical foundation species. Journal of Experimental Biology. 214: 2586-2594.

Jameson, R. J., Kenyon, K. W., Johnson, A. M., and H. M. Wight. 1982. History and status of translocated sea otter populations in North America. Wildlife Society Bulletin. 10(2): 100-107.

Krause-Jensen, D., and C. M. Duarte. 2016. Substantial role of macroalgae in marine carbon sequestration. Nature Geoscience. 9: 737-742.

Lafferty, K. D., and M. T. Tinker. 2014. Sea otters are recolonizing southern California in fits and starts. Ecosphere.5(5).

Laidre, K. L., Jameson, R. J., Gurarie, E., Jeffries, S. J., and H. Allen. 2009. Spatial habitat use patterns of sea otters in coastal Washington. Journal of Marine Mammalogy. 90(4): 906-917.

Redfern et al. 2006. Techniques for cetacean-habitat modeling. Marine Ecology Progress Series. 310: 271-295.

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.

Sunday, J. M., Bates, A. E., and N. K. Dulvy. 2012. Thermal tolerance and the global redistribution of animals. Nature: Climate Change. 2: 686-690.

Wilson, D. E., Bogan, M. A., Brownell, R. L., Burdin, A. M., and M. K. Maminov. 1991. Geographic variation in sea otters, Ehydra lutris. Journal of Mammalogy. 72(1): 22-36.