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sOUTHERN sEA OTTERs: sTUCK IN rECOVErYThough considered a sentinel species for California’s nearshore marine ecosystem, their population numbers have shown little improvement over the years. And because they are more affected by pollutants that pour into the ocean, scientists now wonder if the otter population can recover.

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story by David A. Jessup and Dana Michaels

A sea otter swims to the surface off Monterey with its prize, an abalone, securely clutched in its forepaws.

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The raft of sea otters found regularly in theharbor across from the natural gas poweredelectrical plant at Moss Landing is an example of how closely otters live to intense humanactivity. At right, otters use their high buoyancy to float while they eat and groom themselves. They will wrap themselves in kelp sometimes to maintain their position while eating or grooming.

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For the last 16 years researchers with the Department of Fish and Game have seen the population of southern sea otters vacillate, with the latest three-year average of about 2,600, down again. There are only 600 more otters now than were counted in 1994, when the population

was growing at a steady 4 percent to 5 percent per year. Marine experts expected the population to reach 3,090—a number that would signal recovery—by 2001.

The federal government listed California’s southern sea otter (Enhydra lutris nereis) under the Endangered Species Act in 1977. But despite decades of protection and efforts to start a new population off the Channel Islands, the number of sea otters shows few signs of reaching the recovery criteria for the species any time soon. Sea otters are stuck in recovery largely due to high death rates of prime-aged adult animals. Experts attribute up to 50 percent of sea otter mortality to diseases, parasitism and in-toxications. In the last dozen years, scientists have made connec-tions between whatever it is in the ocean that sickens and kills them to things found on land and related to human activities. Essentially, the cumulative effects of various types of pollution are causing the premature deaths of otters that should live longer and produce more pups.

The story of how the causes of sea otter mortality were dis-covered is an interesting one that shows how patient scientific in-vestigation can reveal complex webs of causality and interaction, and that no isolated discovery could identify the real problem.

From 1992 to 1997 the USGS National Wildlife Health Center in Madison, Wis., performed detailed post mortem examinations

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Most recently, researchers identified anotherserious biotoxin. This one, microtoxin, is more than a thousand times more toxic than domoic acid and is produced by blue-green algae, or cyanobacteria.

on hundreds of sea otters. In 1997, DFG’s Marine Wildlife Veterinary Care and Research Center took over that work and conducted the same ex-aminations on more than 700 otters. The lab also made cursory examinations on thousands more that had been dead for some time. The examina-tions resulted in one of the most detailed and comprehensive cause-of-death assemblages ever developed for any wildlife species. The implica-tions that have come out of those examinations, both for science and for policy decisions in Cali-fornia’s natural resources, are significant.

When sea otter populations started declin-ing in the early 1990s, the first thought was that it must be due to the otters drowning. This had occurred in the late 1970s and early 1980s, and the population did not rebound until California closed most of its near shore gill net fisheries. However, few sea otters examined by veterinary pathologists in the 1990s showed evidence of drowning or of having been captured in nets. The closure of essentially all remaining gill net fisher-ies and added restrictions on pot fisheries for live fish—to protect the fish stocks themselves—did not result in a sea otter recovery.

An early finding was that sea otters were dying of a brain infection caused by a protozoal parasite, Toxoplasma gondii, found in cat feces. The organism is found widely in nature in the muscle tissue of rodents, birds and mammals, but sea otters don’t eat any of those animals; they only eat shellfish. The eggs of

Toxo are only formed in the intestines of cats, shed in feces and are resistant to degradation. They can survive in sulfuric acid or formalin. Experiments showed that Toxo oocysts added to sea water tanks with clean shellfish were readily ingested by blue mussels and could remain infectious in them for months. This is likely true for most filter-feeding bivalves. Thus, it seemed, Toxo must be coming from land sources—either runoff or sewage—and concentrated in shellfish prey. Although native felid species, like bobcat and mountain lion, are competent hosts of Toxoplasma gondii, the introduction of millions of domestic cats into Califor-nia over the last 150 years added to the problem and occurred at a time when sea otters were recovering from the brink of extinc-tion. These findings garnered nationwide media attention and many people thought, “Okay, problem solved.” But it wasn’t that simple.

The Real ProblemBy the late 1990s, it became clear there was another cause

of fatal protozoal brain infections found in sea otters: Sarcocystis neurona. Although similar to Toxo, Sarcocystis neurona’s only

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definitive egg shedding host is the Virginia opossum. Opossums were introduced into California early in the last century. This

second cause of parasitic brain infection in sea otters also has connections to land mammals, as both cats and opossums are non-native and invasive species that thrive in developed areas.

By the early 2000s it appeared that up to 20 percent of adult southern sea otters could be dying of these two protozoal parasites.

It also appeared that both could cause enough brain damage to leave the otters unable to function well enough to detect an approaching shark or boat. But it also became clear that many sea otters survived infection with Toxo and Sarco; that in some years these parasites killed relatively few otters and that they alone were not enough to explain the failure of the population to thrive.

Researchers began asking what other things in sewage, like bacteria, could cause such fatal reactions. Indeed, as investigations progressed, several bacteria associated with human and animal fe-ces were shown to kill sea otters or make them sick. Some of these bacteria caused food poisoning or severe diarrhea in people and domestic animals. They were found to be more prevalent near river mouths, outfalls and in waters off more populated parts of the Central Coast, notably Morro and Monterey bays. Again, a connection to land and people existed, but it didn’t explain why otter populations in more pristine areas were also dying.

In April 2003, a sea otter die-off occurred that was so severe it spurred a federal declaration of a “marine mammal unusual mor-tality event.” In that year many southern sea otter deaths were

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Researching the Challenges Facing California’s Southern Sea Otters

linked to ingestion of domoic acid, a biotoxin that is produced by a red tide organism. It now appears that red tides are influenced by nutrient loading of coastal waters, with urea being the most important source of nitrogen for blooms and toxin production. Urea is the nitrogen in urine that is produced by land mammals and people. It’s also used as a fertilizer.

Through a series of scientific publications, it was also becom-ing increasingly apparent that most persistent organic pollut-ants, like DDT and PCBs, and other contaminants of ecological concern could consistently be found in the blood of live—and liver samples of dead—southern sea otters at levels up to 50 times higher than in northern sea otters (Enhydra lutris kenyoni) from more pristine areas of Alaska.

Some sources of pollutants and contaminants are well-known through the legacy of historic farm and industrial uses. Other, newer contaminants found in otters are plasticizers and solvents. Their effects are poorly understood, but are thought to involve disruption of endocrine hormones in many species. Like the diseases, sea otter contaminant problems appear to be worse in harbors, near river mouths and bays. And like diseases, they apparently move from land to sea.

Most recently, researchers identified another serious bio-toxin. This one, microtoxin, is more than a thousand times more toxic than domoic acid and is produced by blue-green algae, or cyanobacteria. Experts blame this toxin for major salmon die-offs in the Klamath River. It’s potentially lethal to any animal that ingests it. Die-offs of sea otters in 2007 helped identify its presence in Monterey Bay—a first, as it had never before been found in marine animals. Researchers tested waters upstream of the Pajaro River mouth where the first otters were found and identified

Miller, M.A.,I.A. Gardner, D. Paradies, K. Worcester, D. Jessup, E. Dodd, M. Harris, J. Ames, A. Pack-ham, P.A. Conrad. 2002. Coastal freshwater runoff is a risk factor for Toxoplasma gondii in-fection of southern sea otters (Enhydra lutris nereis). International Jour. Parasit. 32:997-1006.

Miller, M.A., I.A. Gardner, A. Packham, J.K. Mazet, K.D. Hanni, D. Jessup, J. Estes, R. Jameson, E. Dodd, B.C. Barr, L.J. Lowenstine, F.M. Gulland, P.A. Conrad. 2002. Evaluation of anindirect fluorescent antibody test (IFAT) for demon-stration of antibodies to Toxoplasma gondii in the sea otter (Enhydra lutris). Journal of Parasi-tology. 88:594-599.

Kreuder, C., M. Miller, D. Jessup, L. Lowenstine M.D. Harris, J. Ames, T.E. Carpenter, P.A. Conrad, J.K. Mazet. 2003. Patterns of mortality in the south-ern sea otter (Enhydra lutris) from 1998-2001. J Wildl. Dis. 39(3): 495-509.

Hanni, K.D., J.A.K. Mazet, F.M.D. Gulland, J. Estes, M. Staedler, M.J. Murray, D.A. Jessup. 2003. Clinical pathological values and assessment of patho-gen exposure in southern and Alaskan sea ot-ters. J. Wildl. Dis. 39(4): 837-850.

Kannan, K., H. Nakata, N. Kajiwara, M. Watanabe, N.J. Thomas, D.A. Jessup, S. Tanabe. 2003. Profiles of polychlorinated biphenyl congeners, or-ganochlorine pesticides and butyltins in south-ern sea otters and their prey: Implications for PCB metabolism. Environmental Toxicology and Chemistry. 23(1): 49-56.

Stavely C.M., K.B. Register, M.A. Miller, S.L. Brock-meier, D.A. Jessup, S. Jang. 2003. Molecular and antigenic characterization of Bordetella bron-chiseptica isolated from a wild southern sea otter (Enhydra lutris nereis) with severe suppu-rative bronchopneumonia. Journal of Veterinary Diagnostic Investigation. 15(6): 570-574.

Gerber L.R., M.T. Tinker, D.F. Doak, J.E. Estes, D.A. Jessup. 2004. Mortality sensitivity in life-stage simulation analysis: A case study of Southern sea otters. Ecological Applications, 14(5): 1154-1165.

Jessup, D.A., M. Miller, J. Ames, M. Harris, P. Conrad C. Kreuder, J.A.K. Mazet. 2004. The southern sea otter (Enhydra lutris nereis) as a sentinel of marine ecosystem health. Ecohealth. 1(3):239-245.

Miller M.A., M.E. Griggs, C. Kreuder, E.R. James, A.C. Melli, P.R. Crosbie, D.A. Jessup, J.C. Boothroyd,

DFG RESEARCHContinued on Page 15

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While considered one of the smallest marine mammals, a male adult can weigh between 70 to 90 pounds and reach from 4 to 5 feet long. Females weigh 30 to 70 pounds and will reach from 3 to 4 feet in length. They will eat up to 25 percent of their own body weight daily. To hold their position as they eat or groom, otters will wrap themselves with kelp. When eating, otters frequently roll in the water as a means to wash food scraps from their fur.

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death can be seen as resulting from pollution and environmental degradation. Ultimately, the contamination threatens not only sea otter health but the health and stability of the entire near shore marine ecosystem. With that goes people’s ability to enjoy and use the ocean.

Is There a Solution?Cleaning up storm drain and agricultural run-off, as well as

nutrient pollution and sewage are ecological and engineering problems that will require significant social, political and finan-cial resources. There remains a tremendous need to inform people of what is at stake so they are able to make the legal, social and financial decisions necessary to curb these various forms of pol-lution.

DFG started this year developing a major public outreach program with its partners USGS, U.S. Fish and Wildlife Service, Monterey Bay Aquarium and the Universatires of California, Santa Cruz and Davis. Primary funding came through the Luck-enbach Oil Spill Settlement Fund established by DFG’s Office of Spill Prevention and Response.

The outreach effort expects to launch a comprehensive website, www.seaotters.com, in the fall of 2011. Seminars have been conducted for the public and a kiosk is being built at the Sey-mour Marine Discovery Center in Santa Cruz. The Monterey Bay Aquarium and Defenders of Wildlife have adapted information provided by DFG into their own public outreach efforts. All the educational materials are being produced in English and Spanish.

While that message will produce dividends in the future, those who understand the serious risks that face sea otters under-stand a more immediate effort is vital to control the killing pol-lutants. Earlier this year, the authority to regulate the discharge of microcystin toxins came under the federal Environmental Protection Agency and the State Water Board. Today, DFG works with state and regional water boards to identify sources of infec-tious organisms, toxins and nutrients. To solve the problems, the various sources of pollution, including runoff, must be better regulated with enforcement of all necessary regulations.

Other suggestions coming from environmental experts include ecological buffer strips, fallow agricultural land and arti-ficial marshes, all designed to catch and clean storm waters before they flush into the ocean. Some environmentally savvy Southern California builders are taking the lead and have begun substitut-ing semi-permeable surfaces for traditional concrete or asphalt.

The key, say scientists who have studied sea otters, is to not allow the situation to progress unchecked, the way some say it had along parts of the East Coast or the Gulf of Mexico. Sea otters are not only a sentinel, a threatened and ecological keystone species, they are one of the reasons tourists love and visit coastal California. If California can’t or won’t save sea otters, what can it save?

David A. Jessup, DVM, MPVM, Dipl. ACZM, retired after 33 years with DFG, 19 of those with OSPR and more than 13 with the Marine Wildlife Veterinary Care and Research Center in Santa Cruz.Dana Michaels is an information officer with the Office of Communications, Education and Outreach.

massive amounts of toxin in Santa Cruz County’s Pinto Lake and, in decreasing amounts, down the Corralitos Creek drainage to the Pajaro. By going back and testing tissues from sea otters examined in earlier years, DFG verified at least 21 sea otters died from lower levels of these toxins from 2004 to 2009. Microtoxins are con-centrated by shellfish—particularly the popular dining variety of oysters, clams and mussels. The toxin can cause acute damage to the heart, liver and brain or more chronic damage that may shorten life.

All along there had been concerns about the potential effects of depletion of favored food items and marginal nutrition on sea otters and their susceptibility to disease. Recently studies by USGS and the University of California-Davis’ School of Veteri-nary Medicine’s Wildlife Health Center have shown that otters in Monterey and Estero bays that eat certain types of snails, clams and mussels, as well as innkeeper worms, have a higher risk of being exposed to Toxo and Sarco. Otters that ate abalone did not face this risk. Other studies showed that these same food items concentrate organic pollutants 10 times greater than in crabs and squid. Filter feeders also concentrate many of the pathogenic bacterial organisms and biotoxins. If food limitation forces otters to shift to less-preferred prey, that may not only have nutritional consequences but may also play a significant role in the diseases and toxins they are exposed to. In other words, in terms of sea ot-ter health, they are what they eat.

Studies of genetics and immune function did not reveal ap-parent connections between inbreeding and lowered resistance to infection or evidence of reduced immune function. But sea ot-ters’ immune systems have had little time to adapt to Toxoplasma and Sarcocystis, or to classic organic chemical pollutants, or for that matter to biotoxins resulting from harmful algal blooms fos-tered by the release of nutrients and other pollutants associated with sewage, agriculture, landscaping, streets and sidewalks.

Some aspects of sea otter biology may make them especially vulnerable to infections and intoxications from polluted runoff. They feed near shore, often within or adjacent to coastal surface water plumes. They may rest and forage in sheltered bays near cities. They have very high metabolic rates and consume up to 30 percent of their body weight daily in invertebrate prey. These attributes have made them a nearly ideal sentinel species for near shore marine ecosystem health studies in California. Yet we now believe they are also a reason the otter population is not recover-ing.

Researchers understand now that southern sea otters seldom die of only one cause. Otters with active protozoal encephalitis may also have high levels of domoic acid in urine. Otters with intoxication or brain infection may not be able to detect an approaching shark or boat. Many pollutants and environmental contaminants are found in dead otters at high levels, but their specific contribution to the manner of death, if any, remains un-clear. When adult mortality in a wildlife population meets or ex-ceeds the rate at which young animals are produced, population growth stagnates or declines. Taken collectively, the southern sea otters’ diseases, parasites and intoxications are strong enough to stop population growth and to cause periodic die-offs. Ad-ditionally, many of the otters’ problems appear to have human connections and they flow from land to sea. All these causes of

Many pollutants and environmental contaminants are found in dead otters at high levels, but their specific contribution to the manner of death, if any, remains unclear.

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D. Brownstein, P.A. Conrad. 2004. An unusual genotype of Toxoplasma gon-dii is common in California sea otters (Enhydra lutris nereis) and is associ-ated with mortality. Int. Jour. Parasit. 34:275-284.

Kreuder, C.K., M. Miller, P. Conrad, L. Low-enstine, T. Carpenter, D.A.Jessup, J.K. Mazet. 2005. Evaluation of cardiac le-sions and risk factors associated with myocarditis and dilated cardiomyopa-thy in southern sea otters (Enhydra lu-tris nereis). AJVR, 66(2):289-299.

Miller, W.A., M.A. Miller, I.A. Gardner, E.R. Atwill, A.C. Melli, M. Harris, J. Ames, K. Worcester, N. Barnes, D. Jessup, P.A. Conrad. 2005. New genotypes and factors associated with Cryptospo-ridium detection in mussels (Mytilus spp.) along the California coast. Int. Jour. Parasitol, 35:1103-1113.

Miller, W., M. Miller, I. Gardner, R. Atwill, B. Byrne, S. Jang, M. Harris, J. Ames, D. Jessup, D. Paradies, K. Wocester, A. Melli, P. Conrad. 2006. Salmonella spp., Vibrio spp., Clostridium perfin-gens, and Plesiamonas shigelloides in marine and freshwater invetebrates from coastal California ecosystems. Microb. Ecol. 52:198-206

Conrad, P.A., M.A. Miller, C. Kreuder, E.R. James, J. Mazet, H. Dabritz, D.A. Jessup, F. Gulland, M.E. Grigg. 2006. Transmis-sion of Toxoplasma: Clues from sea ot-ters as sentinels of Toxoplasma gondii flow into the marine environment. Int. Jour. Parasitol. 35, 1155-1168.

Levin, M., H. Leibrecht, C. Mori, D. Jessup, S. De Guise. 2007. Immunomodulato-ry effects of organochlorine mixtures upon in vitro exposure of peripheral blood leukocytes differ between free-ranging and captive Southern sea otters (Enhydra lutris). Vet. Immu-no. Immunopath. 119:269-277.

Jessup, D.A., M. Miller, C. Kreuder-Johnson, P. Conrad, T. Tinker,J. Estes, J. Mazet. 2007. Sea otters in a dirty ocean. Jour. Am. Vet. Med. Assoc. 231:11, 1648-1652

Aguilar, A., D.A. Jessup, J. Estes, J.C. Garza. 2008. The distribution of nuclear genetic variation and the historical demography of sea otters (Enhydra lu-

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tris). Animal Conservation. 11: 35-45.Miller, M.A., W.A. Miller, P.A. Conrad, E.R.

James, A.C. Melli, C.M. Leutenegger, H.A. Dabritz, A.E. Packham, D. Par-adies, M. Harris, J. Ames, D.A. Jessup, K. Worcester, and M.E. Grigg. 2008. Type X Toxoplasma gondii in wild mus-sel and terrestrial carnivores from coastal California: New linkages be-tween terrestrial mammals, runoff and toxoplasmosis of sea otters. Int. J.Parasitol. 38(11), 1319-1328.

Miller, M., P. Conrad, E.R. James, A. Pack-ham, S. Toy-Choutka, M.J. Murray, D. Jessup, M. Grigg. 2008. Transplacental toxoplasmosis in a wild southern sea otter (Enhydra lutris nereis). Vet. Para-sitol. 153(1-2), 12-18.

Johnson, C.K., M.T. Tinker, J.E. Estes, P.A. Conrad, M. Staedler, M.M. Miller, D.A. Jessup, J.A.K. Mazet. 2008. Prey choice and habitat use drive sea otter patho-gen exposure in a resource-limited coastal system. PNAS: Biological Sci-ences-Ecology 106(7); 2242-2247.

Jessup, D.A., M. H. Ziccardi. 2009. Getting out the oil, twenty years after Exxon Valdez, new ways to treat oiled sea otters. Wildlife Professional 3(2):36-40

Jessup, D.A., M.J. Murray, D.R. Casper, D. Brownstein, C. Kreuder-Johnson. 2009. Canine distemper vaccination is a safe and useful preventive proce-dure for southern sea otters (Enhydra lutris neries). Jour. Zoo and Wildl. Med. 40(4): 705-710.

Miller, M.A., B.A. Byrne, S.S. Jang, E.M. Dodd, E. Dorfmeier, M.D. Harris, J. Ames, D. Paradies, K. Worcester, D.A. Jessup, W. A. Miller. 2009. En-teric bacterial pathogen detection in southern sea otters (Enhydra lutris nereis) is associated with coastal ur-banization and freshwater runoff. Veterinary Research. 41:01. doi:10:105/vetres/2009049

Miller, M.A., B.C. Barr, R. Nordhausen, P. Conrad, E.R. James, M. Murray, A.E. Packham, A.C. Melli, S. Toy-Chaoutka, D. Jessup, M. Grigg. 2008. Ultrastruc-tural and molecular confirmation of the development of Sarcocystis neruo-na tissue cysts in the central ner-

vous system of southern sea otters (Enhydra lutris neries). Int. J. Parasitol. 39(12):1363-1372.

Levin, M., J. Dhanashree, A. Draghi II, F.M. Gulland, D. Jessup, S. De Guise. 2010. Immunomodulatory effects of do-moic acid in California sea lions and Southern sea otters. J. Wildl. Dis. 46(2): 541-550.

Jessup, D.A., C. Johnson, J. Estes, D. Carl-son-Bremer, W.M. Jarman, E. Dodd, T. Tinker, M. Ziccardi. 2010. Persistent organic pollutants in blood of free ranging sea otters (Enhydra lutris) in Alaska and California. J. Wildl. Dis. 46(4) 1214-1253

Miller, M., R.M. Kudela, A. Mekebri, D. Crane, S.C. Oates, M.T. Tinker, M. Staedler, W.A. Miller, S. Toy-Choutka, C. Dominick, D. Hardin, G. Langlois, M. Murray, K. Ward., D. Jessup. 2010. Evi-dence for a novel form of harmful al-gal bloom: Cyanotoxin transfer from land to sea otters. PLoS One 5(9) doi:101371/journal/pone/0012576.

Miller, M. A., P.A. Conrad, M. Harris, B. Hat-field, G. Langlois, D.A. Jessup, S. Maga-ral, A.E. Packham, S. Toy-Choutka, A.E. Melli, M.A. Murray, F.M. Gulland, and M.E. Grigg. 2010. A protozoal-asso-ciated epizootic impacting marine wildlife: Mass-mortality of southern sea otters (Enhydra lutris nereis) due to Sarcocystis neurona infection. Veteri-nary Research. Veterinary Parasitol-ogy 172(3-4): 183-194.

Goldstein, T., A.M. Doroff, P. Toumi, D. Monson, V.A. Gill, A. Burdin, P.A. Con-rad, J.H. Dunn, C. Fields, C. Kreuder, D.A. Jessup, J. Bodkin, J.A. Estes. 2011. Comparison of health and disease exposure in sea otter (Enhydra lutris) populations in Kodiak Island, Alaska and Bering Island, Russia adjacent to the declining Southwest population in Alaska. J. Wildl. Dis. 47(1).

Brownstein, D., M.A. Miller, S. Oates, B. Byrne, S. Jang, M.J. Murray, D.A. Jessup. 2011. Antimicrobial susceptibility of bacterial isolates from southern sea otters (Enhydra lutris nereis). J. Wildl. Dis. 47(2).

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