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:

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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.

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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.

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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.

Knowing me, knowing you: the fate of the toninha, a small dolphin endemic to the Western South Atlantic

By Salvatore Siciliano (1,2)

(1) Laboratório de Enterobactérias, Oswaldo Cruz Institute/Fiocruz, Rio de Janeiro, Brazil
(2) Grupo de Estudos de Mamíferos Marinhos da Região dos Lagos (GEMM-Lagos)

 

 

Background information on Pontoporia blainvillei

The toninha (Pontoporia blainvillei) as it is called in Brazil, or franciscana (Fig.01), is a small dolphin endemic to coastal waters of southeastern and southern Brazil, Uruguay and Argentina. It is the only representative of an ancient lineage of odontocetes, once widely spread over the Pacific and Atlantic oceans. Toninhas occur in waters shallower than 30 m and present a discontinuous distribution from Itaúnas, Brazil (18º 25’S) to Golfo San Matías, Argentina (42º 10’S). The species is considered one of the most threatened small cetaceans in South America due to high, and possibly unsustainable, bycatch levels as well as increasing habitat degradation. Incidental catches in fishing gear, especially gillnets and trammel nets, have been reported along most of the species’ range since at least the 1940s. Other rapidly-increasing conservation issues of significant importance for the franciscana in this region include: (1) habitat degradation, (2) underwater noise, (3) chemical pollution from industrial and urban wastewater, (4) activities related to the exploration and production of oil and gas, and (5) vessel traffic. P. blainvilleiis currently listed as ‘Vulnerable’ in the IUCN Red List of Threatened Species and ‘Critically Endangered’ by the Brazilian Government.

 

Figure 01: A young Pontoporia blainvillei incidentally caught in gillnets set off the northern coast of the state of Rio de Janeiro, Brazil (December 2011).

 

In order to guide conservation and management actions on a regional basis, the franciscana range was divided into four zones, known as ‘Franciscana Management Areas’ (FMAs), in the early 2000s. FMA I includes Espírito Santo (ES) and northern Rio de Janeiro (RJ), states located in southeastern Brazil. FMA II corresponds to southern RJ, São Paulo (SP), Paraná (PR) and northern Santa Catarina (SC) states, in southeastern and southern Brazil. FMA III encompasses southern SC and Rio Grande do Sul (RS) states, in southern Brazil, in addition to Uruguay. The last FMA, the FMA IV, corresponds to the Argentina coast (Fig.02).

The absence of stranded or incidentally killed animals indicates a gap of approximately 320 km in the franciscana distribution between northern and southern RJ. This gap separates the southern border of FMA I and the northern border of FMA II.

 

Figure 02: The FMA areas (in blue) in P. blainvillei distribution range, and the gaps (in white) in toninha distribution along the Northern limit of its distribution in Southeastern Brazil.

 

The toninha is usually very shy and, for this reason, quite difficult to be seen in the wild. More recently, researchers and citizen science projects have succeeded in obtaining very nice pictures of these animals (Fig.03), which are aiding in elucidating the species mysterious behavior, feeding activity and their preferred habitat conditions.

Figure 03: Toninhas in their natural environment along shallow waters off northern São Paulo state, in the summer of 2019. Photo courtesy of Júlio Cardoso, Baleia à Vista Project.

 

Figure 04: Aerial view of the Restinga de Jurubatiba National Park and its adjacent waters, the main toninha habitat along the northern coast of Rio de Janeiro. Photo by Salvatore Siciliano (November 2017).

 

Threats to P. blainvillei along the Brazilian coast

Gillnets are still the main cause of toninha mortality along its entire range. They can be used at the surface or placed at the bottom of the ocean to catch fish, but these nets also entangle this small dolphin (Fig.05, Fig.06).

Figure 05: Gillnets, used at the surface or placed at the bottom of the ocean.

 

Figure 06: Data on gillnet incidental captures of toninhas (Pontoporia blainvillei) along the northern coast of Rio de Janeiro state collected since1988. Note the concentration of records in the Macaé – Quissamã and Cabo de São Thomé areas, adjacent to the Restinga de Jurubatiba National Park. Data on captures come from Prof. Ana Paula M. Di Beneditto/CBB/LCA/UENF.

 

Toninhas also face other threats along the Brazilian coast, including environmental chemical contamination by metals and persistent organic pollutants. These pollutants are persistent in the aquatic ecosystem and may accumulate and magnify throughout the tropic chain, causing deleterious effects in the aquatic fauna. Recently, an ecotoxicological assessment from our research group (GEMM-Lagos/Fiocruz) verified, for the first time, significant intracellular concentrations of several toxic metals, such as Hg and Pb (Fig.07), in P. blainvillei individuals sampled along the coast of the Rio de Janeiro state.

 

Figure 07: Novel HPLC-ICP-MS data on intracellular Pb and Hg in P. blainvillei liver (L), muscle (M) and kidney (K) samples from stranded individuals sampled off the coast of Rio de Janeiro, Brazil.

 

The monitoring of the contaminant levels in toninhas will potentially aid in conservation efforts, as we can identify which metals are of the most concern, because the intracellular presence of toxic metals indicates high bioavailability, probably leading to deleterious effects.

 

Conservation Efforts

What is a Whale Heritage Site (WHS) and why we are proposing ‘Mosaic Jurubatiba’ as a WHS?

Situated on the Northern coast of Rio de Janeiro state, Brazil, the Jurubatiba region (Fig.04; Fig.08) is now a Candidate Whale Heritage Site (WHS). The area has been termed ‘Mosaic Jurubatiba’ as the candidate site includes not only the Jurubatiba National Park, but also encompasses other significant sites for conservation along the central-north coast that lie across three municipalities: Macaé, Carapebus and Quissamã (Fig.08).

Figure 08: Proposed extension of the Jurubatiba National Park to the adjacent waters, home of a vigorous population of P. blainvillei.
Legend: green – Jurubatiba National Park; red – new terrestrial limit; yellow – new marine limit.

 

The location provides habitat to a diversity of wildlife. When considering cetaceans, the most regularly seen individuals are the humpback whales, the Guiana dolphins and the toninhas. This is an important site since it is part of the migration route of humpback whales from their breeding and calving grounds, in warm tropical waters, to their feeding grounds, in Antarctica. In addition, this locality is a significant habitat for the toninha, a restricted range species, and the Guiana dolphin, a data deficient species and, therefore, of great concern. The importance of the site becoming a fully accredited WHS is, therefore, evident to further conserve these species and their habitats.

There is a significant amount of active conservation in the Jurubatiba National Park. The Park is the first to exclusively comprise the Restinga ecosystem. Researchers worked alongside authorities and large organizations, such as IBAMA (Brazilian Ministry of Environment and the federal government), to achieve its national park status.

Figure 09: Outreach material produced for the campaign ‘Mosaic Jurubatiba’ to promote education and conservation of the Toninha.

 

In Quissamã, warning signs were placed along the beaches to alert the population of the importance of the coastal waters as habitat for dolphin species, especially the toninha. This type of cooperation and support of the government and other authorities will aid the candidate site to achieve a full status of WHS.

The long-term goals of the candidate site are to influence the transition away from fishing as a livelihood and to instead embrace the use of responsible tourism to make a living.

 

For more information on Whale Heritage Sites around the world, visit:

http://worldcetaceanalliance.org/

http://whaleheritagesites.org/candidate-site-jurubatiba/

 

For more information on the GEMM-Lagos Project:

contact:gemmlagos@gmail.com

visit their Instagram: toninha_cade_vc

 

Here you can also find a list of some of the Salvatore Siciliano’s publications on Pontoporia blainvillei:

  • Siciliano S, de Moura JF, Tavares DC, Kehrig HA, Hauser-Davis RA, Moreira I, Lavandier R, Lemos LS, EMin-Lima R, Quinete N. 2018. Legacy Contamination in Estuarine Dolphin Species From the South American Coast. In book: Marine Mammal Ecotoxicology. Eds. Fossi MC, Panti C. Publisher: Academic Press.
  • Baptista G, Kehrig HA, Di Beneditto APM, Hauser-Davis RA, Almeida MG, Rezende CE, Siciliano S, de Moura JF and Moreira I. 2016. Mercury, selenium and stable isotopes in four small cetaceans from the Southeastern Brazilian coast: Influence of feeding strategy. Environmental Pollution 218:1298-1307.
  • Frainer G, Siciliano S, Tavares DC. 2016. Franciscana calls for help: the short and long-term effects of Mariana’s disaster on small cetaceans of South-eastern Brazil. International Whaling Commission SC/66b/SM/04. Bled, Slovenia.
  • Lavandier R, Arêas J, Quinete N, de Moura JF, Taniguchi S, Montone RC, Siciliano S, Moreira I. 2015. PCB and PBDE levels in a highly threatened dolphin species from the Southeastern Brazilian coast. Environmental Pollution 208.
  • Lemos LS, de Moura JF, Hauser-Davis RA, de Campos RC, Siciliano S. 2013. Small cetaceans found stranded or accidentally captured in southeastern Brazil: Bioindicators of essential and non-essential trace elements in the environment. Ecotoxicology and Environmental Safety 97:166-175.
  • de Moura JF, Rodrigues ES, Sholl TGC, Siciliano S. 2009. Franciscana dolphin (Pontoporia blainvillei) on the north-east coast of Rio de Janeiro State, Brazil, recorded during a long-term monitoring programme. Marine Biodiversity Records 2:e66.