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.

Who am I?

By Leila Lemos, PhD Student
(hopefully PhD candidate soon)

 

Here I am with the first GEMM Lab blog post of 2018.

Many people begin a New Year thinking about the future and planning goals to achieve in the following year, and that’s exactly how I am starting my year. After two and a half years of my PhD program, my classes and thesis project are nearing the end. However, a large hurdle stands between me and my finish line: my preliminary exams (as opposed to final exams that happen when I defend my thesis).

Oregon State University requires two sets of preliminary examinations (a.k.a. “prelims”) in order to become a PhD candidate. Thus, planning my next steps is essential in order to accomplish my main objective: a successful completion of these two exams.

The first set of exams comprises written comprehensive examinations to be taken over the course of a week (Monday to Friday), where each day belongs to a different member of my committee. The second type of exam is an oral preliminary examination, conducted by my doctoral committee. The written and oral prelims may cover any part of my proposed research topic as described in the proposal I submitted during my first PhD year.

In order to better understand this entire process, I met with Dr. Carl Schreck, a Fisheries and Wildlife Department professor and one of the members of my committee. He has been through this prelim process many times with other students and had good advice for me regarding preparation. He told me to meet with all of my committee members individually to discuss study material and topics. However, he said that I should first define and introduce myself with a title to each committee member, so they know how to base and frame exam questions. But, how do I define myself?

How do you define yourself?
Source: www.johngarvens.com/wpcontent/uploads/2013/02/how_do_you_ define_yourself.jpeg

 

As part of my PhD committee, Dr. Schreck is familiar with my project and what I am studying, so he suggested the title “Conservation Physiologist”. But, do I see myself as a Conservation Physiologist? Will this set-up have implications for my future, such as the type of job I am prepared for and able to get?

I can see it is important to get this title right, as it will influence my exam process as well as my scientific career. However, it can be hard and somewhat tricky when trying to determine what is comprised by your work and what are the directions you want to take in your future. I believe that defining the terms conservationist and physiologist, and what they encompass, is a good first step.

To me, a conservation specialist works for the protection of the species, their habitats, and its natural resources from extinction and biodiversity loss, by identifying and mitigating the possible threats. A conservation specialist’s work can help in establishing new regulations, conservation actions, and management interventions. As for an animal physiology specialist, their research may focus on how animals respond to internal and external elements. This specialist often studies an animal’s vital functions like reproduction, movement, growth, metabolism and nutrition.

According to Cooke et al. (2013), conservation specialists focus on population characteristics (e.g., abundance and structure) and indicators of responses to environmental perturbations and human activities. Thus, merging conservation and physiology disciplines enables fundamental understanding of the animal response mechanisms to such threats. Using animal physiology as a tool is valuable for developing cause-and-effect relationships, identifying stressor thresholds, and improving ecological model predictions of animal responses. Thus, conservation physiology is an inter-disciplinary field that provides physiological evidence to promote advances in conservation and resource management.

My PhD project is multidisciplinary, where the overall aim is to understand how gray whales are physiologically responding to variability in ambient noise, and how their hormone levels vary across individual, time, body condition, location, and noise levels. I enjoy many aspects of the project, but what I find myself most excited about is linking information about sex, age, body condition, and cortisol levels to specific individuals we observe multiple times in the field. As we monitor their change in body condition and hormones, I am highly motivated to build these whale ‘life-history stories’ in order to better understand patterns and drivers of variability. Although we have not yet tied the noise data into our analyses of whale health, I am very interested to see how this piece of the puzzle fits into these whale ‘life-history stories’.

In this study, animal physiology facilitates our stories. Scientific understanding is the root of all good conservation, so I believe that this project is an important step toward improved conservation of baleen whales. Once we are able to understand how gray whales respond physiologically to impacts of ocean noise, we can promote management actions that will enhance species conservation.

Thus, I can confidently say, I am a Conservation Physiologist.

Me, in Newport, OR, during fieldwork in 2017.
Source: Sharon Nieukirk, 2017.

 

Over the next three months I will be meeting with my committee members and studying for my prelims. I hope that this process will prepare me to become a PhD candidate by the time my exams come around in March. Then, I will have accomplished my first goal of 2018, so I can go on to plan for the next ones!

 

References:

Cooke SJ, Sack L, Franklin CE, Farrell AP, Beardall J, Wikelski M, and Chown SL. What is conservation physiology? Perspectives on an increasingly integrated and essential science. Conserv Physiol. 2013; 1(1): cot001. Published online 2013 Mar 13. doi:  10.1093/conphys/cot001.