Southern Sea Otter Rehabilitation: Lessons and Impacts from the Monterey Bay Aquarium
Abstract
:1. Introduction
1.1. Wildlife Rehabilitation
1.2. The Southern Sea Otter
2. Materials and Methods
2.1. The Monterey Bay Aquarium
2.2. Methods
3. Results
3.1. The Program’s Beginnings
3.2. Surrogacy
3.3. Conservation Impact of Releasing Surrogate-Reared Sea Otters
3.4. Collaborative Conservation Research
4. Conclusions
4.1. Key Takeaway
4.2. The Future
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Paterson, J.E.; Carstairs, S.; Davy, C.M. Population-level effects of wildlife rehabilitation and release vary with life-history strategy. J. Nat. Conserv. 2021, 61, 125983. [Google Scholar] [CrossRef]
- Saran, K.A.; Parker, G.; Parker, R.; Dickman, C.R. Rehabilitation as a conservation tool: A case studyusing the common wombat. Pac. Conserv. Biol. 2011, 17, 310–319. [Google Scholar] [CrossRef] [Green Version]
- Miller, E. Minimum Standards for Wildlife Rehabilitation, 4th ed.; National Wildlife Rehabilitators Association: St. Cloud, MN, USA, 2012. [Google Scholar]
- Kelly, G. Importance of taxonomic group, life stage and circumstance of rescue upon wildlife rehabilitation in Ontario, Canada. J. Nat. Conserv. 2020, 57, 125897. [Google Scholar] [CrossRef]
- Molony, S.; Baker, P.; Garland, L.; Cuthill, I.; Harris, S. Factors that can be used to predict release rates for wildlife casualties. Anim. Welf. 2007, 16, 361. [Google Scholar]
- Guy, A.J.; Curnoe, D.; Banks, P.B. A survey of current mammal rehabilitation and release practices. Biodivers. Conserv. 2013, 22, 825–837. [Google Scholar] [CrossRef]
- Karesh, W.B. Wildlife rehabilitation: Additional considerations for developing countries. J. Zoo Wildl. Med. 1995, 26, 2–9. [Google Scholar]
- Astore, V.; Estrada, R.; Jacome, N.L. Reintroduction strategy for the Andean condor conservation program, Argentina. Int. Zoo. Yearb. 2017, 51, 124–136. [Google Scholar] [CrossRef]
- Hogg, C.; Lee, A.; Srb, C.; Hibbard, C. Metapopulation management of an endangered species with limited genetic diversity in the presence of disease: The Tasmanian devil Sarcophilus harrisii. Int. Zoo Yearb. 2017, 51, 137–153. [Google Scholar] [CrossRef]
- Walters, J.R.; Derrickson, S.R.; Michael Fry, D.; Haig, S.M.; Marzluff, J.M.; Wunderle, J.M. Status of the California condor (Gymnogyps californianus) and Efforts to Achieve Its Recovery. Auk 2010, 127, 969–1001. [Google Scholar] [CrossRef] [Green Version]
- Adimey, N.M.; Ross, M.; Hall, M.; Reid, J.P.; Barlas, M.E.; Diagne, L.W.K.; Bonde, R.K. Twenty-six years of post-release monitoring of Florida manatees (Trichechus manatus latirostris): Evaluation of a cooperative rehabilitation program. Aquat. Mamm. 2016, 42, 391. [Google Scholar] [CrossRef]
- Harting, A.L.; Johanos, T.C.; Littnan, C.L. Benefits derived from opportunistic survival-enhancing interventions for the Hawaiian monk seal: The silver BB paradigm. Endanger. Species Res. 2014, 25, 89–96. [Google Scholar] [CrossRef] [Green Version]
- Hatfield, B.B.; Yee, J.L.; Kenner, M.C.; Tomoleoni, J.A. California Sea Otter (Enhydra lutris nereis) Census Results, Spring 2019; U.S. Geological Survey Data Series; U.S. Geological Survey National Center: Reston, VA, USA, 2019.
- United States Fish and Wildlife Service. Southern Sea Otter: 5-Year Review: Summary and Evaluation; U.S. Fish and Wildlife Service Ventura Fish and Wildlife Office: Ventura, CA, USA, 2015; Volume 42.
- Estes, J.A.; Palmisano, J.F. Sea otters: Their role in structuring nearshore communities. Science 1974, 185, 1058–1060. [Google Scholar] [CrossRef]
- Mayer, K.A.; Tinker, M.T.; Nicholson, T.E.; Murray, M.J.; Johnson, A.B.; Staedler, M.M.; Fujii, J.A.; Van Houtan, K.S. Surrogate rearing a keystone species to enhance population and ecosystem restoration. Oryx 2021, 55, 535–545. [Google Scholar] [CrossRef] [Green Version]
- Hughes, B.B.; Eby, R.; Van Dyke, E.; Tinker, M.T.; Marks, C.I.; Johnson, K.S.; Wasson, K. Recovery of a top predator mediates negative eutrophic effects on seagrass. PNAS 2013, 110, 15313–15318. [Google Scholar] [CrossRef] [Green Version]
- Smith, J.G.; Tomoleoni, J.; Staedler, M.; Lyon, S.; Fujii, J.; Tinker, M.T. Behavioral responses across a mosaic of ecosystem states restructure a sea otter–urchin trophic cascade. PNAS 2021, 118, e2012493118. [Google Scholar] [CrossRef]
- Kenner, M.C.; Tinker, M.T. Stability and change in kelp forest habitats at San Nicolas Island. West. N. Am. Nat. 2018, 78, 633–643. [Google Scholar] [CrossRef]
- Estes, J.A.; Terborgh, J.; Brashares, J.S.; Power, M.E.; Berger, J.; Bond, W.J.; Carpenter, S.R.; Essington, T.E.; Holt, R.D.; Jackson, J.B. Trophic downgrading of planet Earth. Science 2011, 333, 301–306. [Google Scholar] [CrossRef] [Green Version]
- Miller, M.A.; Moriarty, M.E.; Henkel, L.; Tinker, M.T.; Burgess, T.L.; Batac, F.I.; Dodd, E.; Young, C.; Harris, M.D.; Jessup, D.A. Predators, disease, and environmental change in the nearshore ecosystem: Mortality in southern sea otters (Enhydra lutris nereis) from 1998–2012. Front. Mar. Sci. 2020, 7, 582. [Google Scholar] [CrossRef]
- Nicholson, T.E.; Mayer, K.A.; Staedler, M.M.; Fujii, J.A.; Murray, M.J.; Johnson, A.B.; Tinker, M.T.; Van Houtan, K.S. Gaps in kelp cover may threaten the recovery of California sea otters. Ecography 2018, 41, 1751–1762. [Google Scholar] [CrossRef] [Green Version]
- Thometz, N.; Staedler, M.; Tomoleoni, J.; Bodkin, J.L.; Bentall, G.; Tinker, M.T. Trade-offs between energy maximization and parental care in a central place forager, the sea otter. Behav. Ecol. 2016, 27, 1552–1566. [Google Scholar] [CrossRef] [Green Version]
- Cortez, M.; Wolt, R.; Gelwick, F.; Osterrieder, S.K.; Davis, R.W. Development of an altricial mammal at sea: I. Activity budgets of female sea otters and their pups in Simpson Bay, Alaska. J. Exp. Mar. Biol. Ecol. 2016, 481, 71–80. [Google Scholar] [CrossRef]
- Nicholson, T.E.; Mayer, K.A.; Staedler, M.M.; Johnson, A.B. Effects of rearing methods on survival of released free-ranging juvenile southern sea otters. Biol. Conserv. 2007, 138, 313–320. [Google Scholar] [CrossRef]
- Riedman, M.L.; Estes, J.A.; Staedler, M.M.; Giles, A.A.; Carlson, D.R. Breeding patterns and reproductive success of California sea otters. J. Wildl. Manag. 1994, 58, 391–399. [Google Scholar] [CrossRef]
- Ralls, K.; Siniff, D.B.; Williams, T.D.; Kuechle, V. An intraperitoneal radio transmitter for sea otters. Mar. Mamm. Sci. 1989, 5, 376–381. [Google Scholar] [CrossRef]
- Johnson, A.; Mayer, K. The value of rescuing, treating, and releasing live-stranded sea otters. In Sea Otter Conservation; Elsevier: Amsterdam, The Netherlands, 2015; pp. 235–255. [Google Scholar]
- Tama, J. Crises, commissions, and reform: The impact of blue-ribbon panels. PRQ 2014, 67, 152–164. [Google Scholar] [CrossRef]
- Kenyon, K. The Sea Otter in the Eastern North Pacific; Dover Publications: New York, NY, USA, 1975. [Google Scholar]
- Staedler, M.M.; Riedman, M.L. A case of adoption in the California Sea Otter. Mar. Mamm. Sci. 1989, 5, 391–394. [Google Scholar] [CrossRef]
- Nicholson, T.; Mayer, K.; Hazan, S.; Murray, M.; Van Houtan, K.S.; DeAngelo, C.; Fujii, J. Advancing surrogate-rearing methods to enhance southern sea otter recovery. Biol. Conserv. 2022; in review. [Google Scholar]
- Siniff, D.B.; Ralls, K. Reproduction, survival and tag loss in California sea otters. Mar. Mamm. Sci. 1991, 7, 211–299. [Google Scholar] [CrossRef]
- Tinker, M.T.; Hatfield, B.B. Annual California Sea Otter Census—1985–2019 Spring Census Summary; U.S. Geological Survey: Santa Cruz, CA, USA, 2019. [CrossRef]
- Hughes, B.B.; Wasson, K.; Tinker, M.T.; Williams, S.L.; Carswell, L.P.; Boyer, K.E.; Beck, M.W.; Eby, R.; Scoles, R.; Staedler, M. Species recovery and recolonization of past habitats: Lessons for science and conservation from sea otters in estuaries. PeerJ 2019, 7, e8100. [Google Scholar] [CrossRef]
- Bowen, L.; Miles, A.K.; Murray, M.; Haulena, M.; Tuttle, J.; Van Bonn, W.; Adams, L.; Bodkin, J.L.; Ballachey, B.; Estes, J. Gene transcription in sea otters (Enhydra lutris); development of a diagnostic tool for sea otter and ecosystem health. Mol. Ecol. Resour. 2012, 12, 67–74. [Google Scholar] [CrossRef] [Green Version]
- Hanni, K.D.; Mazet, J.A.; Gulland, F.M.; Estes, J.; Staedler, M.; Murray, M.J.; Miller, M.; Jessup, D.A. Clinical pathology and assessment of pathogen exposure in southern and Alaskan sea otters. J. Wildl. Dis. 2003, 39, 837–850. [Google Scholar] [CrossRef] [Green Version]
- Tyrrell, L.P.; Newsome, S.D.; Fogel, M.L.; Viens, M.; Bowden, R.; Murray, M.J. Vibrissae growth rates and trophic discrimination factors in captive southern sea otters (Enhydra lutris nereis). J. Mammal. 2013, 94, 331–338. [Google Scholar] [CrossRef]
- Jessup, D.A.; Yeates, L.C.; Toy-Choutka, S.; Casper, D.; Murray, M.J.; Ziccardi, M.H. Washing oiled sea otters. Wildl. Soc. Bull. 2012, 36, 6–15. [Google Scholar] [CrossRef]
- Murray, M.; Young, M.; Santymire, R. Use of the ACTH challenge test to identify the predominant glucocorticoid in the southern sea otter (Enhydra lutris nereis). Conserv. Physiol. 2020, 8, coz116. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moriarty, M.E.; Tinker, M.T.; Miller, M.A.; Tomoleoni, J.A.; Staedler, M.M.; Fujii, J.A.; Batac, F.I.; Dodd, E.M.; Kudela, R.M.; Zubkousky-White, V. Exposure to domoic acid is an ecological driver of cardiac disease in southern sea otters✰. Harmful Algae 2021, 101, 101973. [Google Scholar] [CrossRef] [PubMed]
- Gunther-Harrington, C.T.; Moriarty, M.E.; Field, C.L.; Adams, L.M.; Johnson, C.K.; Murray, M.J. Transthoracic echocardiographic evaluation and serum cardiac troponin values in anesthetized healthy female southern sea otters (Enhydra lutris nereis). JZWM 2021, 52, 490–498. [Google Scholar] [CrossRef]
- Nicholson, T.E.; Mayer, K.A.; Staedler, M.M.; Gagné, T.O.; Murray, M.J.; Young, M.A.; Tomoleoni, J.A.; Tinker, M.T.; Van Houtan, K.S. Robust age estimation of southern sea otters from multiple morphometrics. Ecol. Evol. 2020, 10, 8592–8609. [Google Scholar] [CrossRef]
- Bodkin, J.; Ballachey, B.; Esslinger, G. Synthesis of nearshore recovery following the 1989 Exxon Valdez oil spill: Trends in sea otter population abundance in Western Prince William Sound. Exxon Valdez 2011, 1-17, 1–17. [Google Scholar]
- Lee, E.; Byrne, B.A.; Young, M.; Murray, M.; Miller, M.; Tell, L.A. Pharmacokinetic indices for cefovecin after single-dose administration to adult sea otters (Enhydra lutris). JVPT 2016, 39, 625–628. [Google Scholar] [CrossRef]
- Miller, M.A.; Moriarty, M.E.; Duignan, P.J.; Zabka, T.S.; Dodd, E.; Batac, F.I.; Young, C.; Reed, A.; Harris, M.D.; Greenwald, K. Clinical signs and pathology associated with domoic acid toxicosis in southern sea otters (Enhydra lutris nereis). Front. Mar. Sci. 2021, 8, 585501. [Google Scholar] [CrossRef]
- Shapiro, K.; Miller, M.A.; Packham, A.E.; Aguilar, B.; Conrad, P.A.; Vanwormer, E.; Murray, M.J. Dual congenital transmission of Toxoplasma gondii and Sarcocystis neurona in a late-term aborted pup from a chronically infected southern sea otter (Enhydra lutris nereis). Parasitology 2016, 143, 276–288. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bowen, L.; Miles, A.K.; Kolden, C.A.; Saarinen, J.A.; Bodkin, J.L.; Murray, M.J.; Tinker, M.T. Effects of wildfire on sea otter (Enhydra lutris) gene transcript profiles. Mar. Mamm. Sci. 2015, 31, 191–210. [Google Scholar] [CrossRef]
- Miles, A.K.; Bowen, L.; Ballachey, B.; Bodkin, J.L.; Murray, M.; Estes, J.; Keister, R.A.; Stott, J.L. Variations of transcript profiles between sea otters Enhydra lutris from Prince William Sound, Alaska, and clinically normal reference otters. Mar. Ecol. Prog. 2012, 451, 201–212. [Google Scholar] [CrossRef]
- Casson, C.J.; Murray, M.; Johnson, A.; Belting, T. Sea Otter (Enhydra lutris) Care Manual; Association of Zoos and Aquariums: Silver Spring, MD, USA, 2019. [Google Scholar]
- Oiled Wildlife Care Network. Protocols for the Care of Oil-Affected Sea Otters (Enhydra lutris); Oiled Wildlife Care Network: Davis, CA, USA, 2020. [Google Scholar]
- Strobel, S.M.; Miller, M.A.; Murray, M.J.; Reichmuth, C. Anatomy of the sense of touch in sea otters: Cutaneous mechanoreceptors and structural features of glabrous skin. Anat. Rec. 2022, 305, 535–555. [Google Scholar] [CrossRef] [PubMed]
- Beichman, A.C.; Koepfli, K.-P.; Li, G.; Murphy, W.; Dobrynin, P.; Kliver, S.; Tinker, M.T.; Murray, M.J.; Johnson, J.; Lindblad-Toh, K. Aquatic adaptation and depleted diversity: A deep dive into the genomes of the sea otter and giant otter. Mol. Biol. Evol. 2019, 36, 2631–2655. [Google Scholar] [CrossRef]
- Wright, T.; Davis, R.W.; Pearson, H.C.; Murray, M.; Sheffield-Moore, M. Skeletal muscle thermogenesis enables aquatic life in the smallest marine mammal. Science 2021, 373, 223–225. [Google Scholar] [CrossRef]
- Strobel, S.M.; Moore, B.A.; Freeman, K.S.; Murray, M.J.; Reichmuth, C. Adaptations for amphibious vision in sea otters (Enhydra lutris): Structural and functional observations. J. Comp. Physiol. A 2020, 206, 767–782. [Google Scholar] [CrossRef]
- Hatfield, B.B.; Ames, J.A.; Estes, J.A.; Tinker, M.T.; Johnson, A.B.; Staedler, M.M.; Harris, M.D. Sea otter mortality in fish and shellfish traps: Estimating potential impacts and exploring possible solutions. Endanger. Species. Res. 2011, 13, 219–229. [Google Scholar] [CrossRef]
- Ralls, K.; Eagle, T.C.; Siniff, D.B. Movement and spatial use patterns of California sea otters. Can. J. Zool. 1996, 74, 1841–1849. [Google Scholar] [CrossRef]
Stranding Cause | Description | No. Cases |
---|---|---|
Pre-mature weaning | Signs of emaciation or stunting due to early weaning or chronic malnutrition during weaning | 38 |
ELS/mating trauma | Significant abrading or loss of nose-pad due to mating trauma (28), emaciation related to late-lactation (3) | 31 |
Anthropogenic Trauma | Laceration, punctures, and fractures consistent with boat strike (2), fisheries interactions/line entanglement (6), tar or oiling (2), nonspecific anthropogenic trauma (5) | 15 |
Neurological disease | Fine muscle tremors, seizures, and/or loss of motor function | 14 |
Acanthocephalan peritonitis | Presence of acanthocephalan parasites | 11 |
Shark bite | Lacerations from attempted depredation | 11 |
Geriatric | Pathology related to old age and poor dentition | 4 |
Other | Storm stress (1), respiratory disease (2), reproductive complications (1) or unknown (18) | 22 |
Total | 146 |
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Konrad, L.; Fujii, J.A.; Hazan, S.; Johnson, A.B.; Mayer, K.A.; Murray, M.J.; Nicholson, T.E.; Staedler, M.M.; Young, C. Southern Sea Otter Rehabilitation: Lessons and Impacts from the Monterey Bay Aquarium. J. Zool. Bot. Gard. 2022, 3, 641-652. https://doi.org/10.3390/jzbg3040047
Konrad L, Fujii JA, Hazan S, Johnson AB, Mayer KA, Murray MJ, Nicholson TE, Staedler MM, Young C. Southern Sea Otter Rehabilitation: Lessons and Impacts from the Monterey Bay Aquarium. Journal of Zoological and Botanical Gardens. 2022; 3(4):641-652. https://doi.org/10.3390/jzbg3040047
Chicago/Turabian StyleKonrad, Leilani, Jessica A. Fujii, Sandrine Hazan, Andrew B. Johnson, Karl A. Mayer, Michael J. Murray, Teri E. Nicholson, Michelle M. Staedler, and Colleen Young. 2022. "Southern Sea Otter Rehabilitation: Lessons and Impacts from the Monterey Bay Aquarium" Journal of Zoological and Botanical Gardens 3, no. 4: 641-652. https://doi.org/10.3390/jzbg3040047
APA StyleKonrad, L., Fujii, J. A., Hazan, S., Johnson, A. B., Mayer, K. A., Murray, M. J., Nicholson, T. E., Staedler, M. M., & Young, C. (2022). Southern Sea Otter Rehabilitation: Lessons and Impacts from the Monterey Bay Aquarium. Journal of Zoological and Botanical Gardens, 3(4), 641-652. https://doi.org/10.3390/jzbg3040047