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.
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).
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.
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.
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.
