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2 Animal Care and Management At the National Zoo responsibility for the care and management of the animal collection resides in the Animal Programs Department, Animal Health Department, and Pathology Department. These departments are generally responsible for the exhibition, day-to-day care, and health of the animal collection (NZP, Best Practices, 2003). The National Zoo's Institutional Animal Care and Use Committees (IACUCs) are responsible for reviewing exhibit, management, and research programs to ensure that animals in the collection and research programs receive humane care and treatment (NZP, General Memorandum No. 15, April 2003, September 2003). The Animal Programs Department is generally responsible for the exhibition of the animals, day-to-day care of the animals, and development of the animal collection (NZP, Department of Animal Programs Best Practices, 2003). The Department of Animal Health consists of the veterinary staff at the animal hospital, as well as the nutrition and commissary staff. This department is responsible for the health of the animal collection: proper nutrition, preventive medicine, and health care (NZP, Department of Animal Health Best Practices, 2003). The Department of Pathology provides clinical laboratory and postmortem diagnosis and research to identify diseases that are occurring at the National Zoo and determine how they can be controlled or prevented (NZP, Department of Pathology Best Practices, 2003). ANIMAL PROGRAMS DEPARTMENT Within the Animal Programs Department, the animal collection is grouped into eight units, by either species type or exhibit location: 1. Cheetahs and Elephants Unit 2. Lions and Tigers Unit 3. Primates and Pandas Unit 4. Small Mammals and Kid's Farm Unit 5. Birds Unit 6. Reptiles Unit 7. Invertebrates Unit 8. Beaver Valley and Amazonia Unit The Animal Programs Department is headed by a general curator, who is assisted by two associate curators, each with oversight responsibility of four units. Each unit is managed by an assistant curator. The eight assistant curators, manage the activities of the animal keepers assigned to each respective unit. Responsibilities for animal care and management are divided among the staff as follows: 23

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24 ANIMAL CARE AND MANAGEMENT AT THE NATIONAL ZOO: INTERIM REPORT Animal Keeper Keepers are responsible for independently providing the day-to-day care and maintenance of animals and the exhibits in which they are housed. Their primary responsibilities include (NZP, Animal Programs Best Practices, Primary Keeper Responsibilities; Position Description Animal Keeper): daily inspections of all animals in their care and reporting of any evidence of illness, injury, or abnormal behavior to the curator and veterinarian. feeding and watering assigned animals, including preparation of food, and placement in animal enclosures. Maintaining current records on food and water consumption and report deviations from normal or expected patterns. daily cleaning of exhibit interiors and exteriors, service areas, and public areas adjacent to the animal enclosure. regularly inspecting and maintaining of exhibit area, including trimming and watering of plants, maintenance of furniture, mechanical and life-support systems, and either correcting or referring the problems to the supervisor. applying the approved enrichment plan for each assigned animal. completing daily reports on assigned animals. Their duties also consist of other activities such as assisting with research and breeding programs, interacting with zoo visitors, and developing training and enrichment programs. Assistant Curator The assistant curators are responsible for the conception, formulation, leadership, and conduct of all animal care, breeding, conservation, exhibition, and associated public education for a designated portion of the animal collection (called a unit). Their primary duties include (Position Description Supervisory Biologist): responsibility for all aspects of the daily care and exhibition of all animals in their assigned unit. With the Nutritionist, developing diet formulations and protocols for diet preparation and presentation; with the heads of the Departments of Animal Health and Pathology, developing and overseeing preventive medical programs for animals in their assigned unit. developing and implementing a detailed collection plan; working with national and international conservation coordinating efforts to identify species and individual animals to be bred and exchanged with other zoo to meet breeding objectives. developing plans for the exhibition of the collection. working with the registrar to provide accurate and timely information for the NZP animal records systems. developing and implementing annual operating budgets. supervising animal keepers, scheduling staff, and appraising performance; training and directing volunteers and interns. formulating, conducting, analyzing, and publishing research studies that are original, hypothesis- driven research related to managerial and education responsibilities; seeking funding to support research; coordinating research of other scientists wishing to use the collection; reviewing research proposals for appropriateness and routing them to the IACUC for approval. working with the Department of Exhibit Interpretation on exhibit materials and providing information for demonstration tours and education materials. serving as spokesperson for public information efforts regarding animals in their designated unit.

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ANIMAL CARE AND MANAGEMENT 25 Associate Curator Each associate curator oversees 50 percent of the animal collection units, with responsibility for the conception, formulation, leadership, and conduct of all animal care, breeding, conservation, exhibition, and associated public education. Specific responsibilities as listed in the NZP Position Description are essentially identical to those described for assistant curators (Position Description Associate Curator). General Curator The general curator has authority and is responsible for participating with and assisting the director and senior management team in the overall planning, direction, and management of NZP programs and activities in the exhibition, study, and care of the living animal collections at the Rock Creek Park facility (Position Description General Curator). VETERINARY CARE Zoos differ from some museums in that they have the challenge of maintaining the health and welfare of living animal collections. Zoo animal medicine has made remarkable advances over the past century, in part because zoos have evolved from mere collections of exotic animals to centers of research in animal biology and disease diagnosis, treatment, and prevention. The first book on zoo animal medicine was written in 1923 (Fox, 1923). Until 1960, when the American Association of Zoo Veterinarians (AAZV) was established, few veterinarians were concerned with wildlife disease and captive animal medicine (Fowler, 1986a). The level of sophistication in zoo animal medicine and husbandry is now such that the care provided to zoo animals is on a level with that provided to companion and other domestic animals. These improvements have resulted not only from research, but also from specialized training of veterinarians in zoo animal medicine, publications devoted to zoo animal medicine, establishment of national zoological organizations, and an increased awareness of both physical and psychological needs of captive wild animals. Zoos are increasingly becoming leaders in the science of conservation biology and in the practice of preserving rare and endangered species and their habitats. Although variation exists between facilities, modern zoos have accepted certain minimum standards (AAZV, 1999; AZA, 2003c) related to the veterinary medical care provided to animals in their collections: An adequate number of technically competent veterinarians (Stetter et al., 2003). An adequate number of trained veterinary technicians and support staff. A well-equipped, well-designed facility that adequately serves the needs of the animals and the staff (Simmons, 2003). A complete and retrievable medical records system. Written protocols and procedures (Janssen et al., 2003). An organizational structure and medical decision process that places the responsibility for animal health with the veterinarians, while seeking input from other professionals including keepers, curators, nutritionists, and others (Stetter et al., 2003; Janssen, et al., 2003). A veterinary department that upholds professional decorum (Janssen, et al., 2003). Access to diagnostic laboratory services. Exceptional modern zoos additionally have veterinarians who have received advanced certification or residency training under the auspices of the American College of Zoological Medicine, the American Veterinary Medical Association, or other professional organization. an active residency training program.

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26 ANIMAL CARE AND MANAGEMENT AT THE NATIONAL ZOO: INTERIM REPORT opportunities, such as public viewing areas, for the public to observe veterinary medical procedures, gain a better understanding of zoo animal medicine, and acquire a greater awareness of preventive medicine and quality of animal care (Stetter, et al., 2000). Preventive Medicine Preventive medical programs include all practices that strengthen genetic and immunologic resistance to disease, provide sound nutrition, and minimize exposure to disease agents (Fowler, 1986b). The ultimate goal of a preventive medicine program is prevention and early detection of disease (Miller, 2000; AAZV, 1999). Fowler describes a sound program as one that involves a written plan, education and training of all parties expected to carry it out, continued monitoring, and persistence in the practice of the plan (Fowler, 1986b). An optimum preventive medicine program is reviewed and upgraded annually to reflect collection and species-specific health concerns (Miller, 2000) and it covers the elements listed in Table 2-1. TABLE 2-1 Elements of an Effective Preventive Medicine Programa Quarantine Twenty years ago the failure to provide adequate facilities and failure to carry out an effective quarantine program were the most glaring deficiencies in zoos in North America, Great Britain, and Western Europe (Fowler, 1986a). Currently zoos are subject to government quarantine procedures as well as to quarantine requirements adopted by the AZA in 1994 (Miller, 1995). The AZA quarantine requirements (AZA, 2003c), as well as quarantine requirements subsequently laid out by the AAZV (1999), detail the most desirable quarantine design, but enacting this design is not always possible because of constraints of cost, facilities, and personnel, and ultimately each zoo has control over its own in-house quarantine program (AAZV, 1999). Parasite Surveillance Procedures and Control - Parasite control is more complicated than the simple periodic administration of anthelmintic preparations. A regular schedule of fecal examinations is important to facilitate the detection and treatment of parasite infections before clinical signs appear. Fecal examinations are also an important part of the quarantine procedure. External parasites, though more difficult to detect, should also be considered during surveillance procedures, Examination for external parasites should be part of a complete physical exam. The movement of animals or exhibit furniture from one exhibit to another needs to be carefully considered to prevent exposure to parasites that could cause a fatal infection (AAZV, 1999). Immunization - Vaccination programs are a key component of preventive medicine programs. The design of these programs varies widely, and is based on the animal collection, diseases endemic to the area and potential for exposure. There is a further challenge in that vaccination recommendations for exotic species are made in most cases by extrapolation rather than through extensive research (AAZV, 1999). Infectious Diseases Screening Monitoring the disease status of an animal collection can allow for early detection of outbreaks of infectious disease within zoos. As with vaccination programs the design of an infectious disease screening program depends on the prevalence of a disease in the vicinity of the zoological park or in the prevalence of the disease within the animal collection (AAZV, 1999). Periodic Reviews of Diets - High-quality nutrition is key to animal health. This includes not only developing a complete and balanced diet acceptable to the animals but also ascertaining that the quality of the feed is acceptable (AAZV, 1999). A proper diet is one with which an animal will attain maximum development, maintain normal weight, breed and rear healthy offspring, and live out a full term of life (Clemens, 1984). As in farming, feed costs are one of the top operational costs (the others being labor and facilities). Periodic Review of Exhibit Design and Husbandry Techniques - A review of exhibit design and animal management should be conducted periodically as part of a preventive medicine program. The design of animal enclosures should allow for public viewing of the animal but should also incorporate aspects of animal and keeper safety. Twenty years ago trauma was the most important cause of mortality in captive

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ANIMAL CARE AND MANAGEMENT 27 wild animals (Griner, 1983), and is still considered a leading cause of zoo animal death today. Review of husbandry techniques, including the proper handling and disposal of animal wastes, food wastes and other debris is important for the control of infectious agents as well as vermin (AAZV, 1999). Periodic Review of Vermin Control - Control of vermin (both vertebrate and invertebrate) is an important part of a preventive medicine programs because of the potential for pests to serve as vectors or reservoirs of disease. Review of the vermin control program should also take into account the types of pesticides being used and the signs of exposure in collection animals (AAZV, 1999). Toxicologic problems are generally not considered a major cause of mortality in zoos, however, it is a major concern. Periodic Review of Mortality and Morbidity A review of mortality and morbidity should be conducted periodically as part of a preventive medicine program. Changes in animal health, nutrition, and husbandry can be initiated in response to trends observed in animal illness or deaths. aAdapted from AAZV (1999) and Fowler, (1986b). Veterinary Care at the National Zoo The National Zoo currently employs three full-time board-certified (by the American College of Zoological Medicine) clinical veterinarians: two individuals at the Rock Creek Park facility and one at the CRC. At the Rock Creek Park facility there are two additional veterinarians: a former veterinary resident, who is on a one-year appointment, and a veterinary resident. In total there are five practicing clinical veterinarians that provide veterinary medical care to the animal collection. A research veterinarian provides additional support to the clinical veterinarian at the CRC when necessary. The Rock Creek Park veterinary staff is supported by three keepers and two veterinary technicians. The CRC veterinarian is supported by one veterinary technician. The keepers are responsible for the daily feeding of the animals currently housed in the hospital, cleaning and maintaining the enclosures, and assisting the veterinarians (NZP, Department of Animal Health Procedures--Hospitalized Animal Procedures, 2003). The veterinary technicians are responsible for ordering and dispensing all pharmaceuticals, documenting anesthesia and prescription records, and providing technical assistance to the veterinary staff (NZP, Department of Animal Health Procedures--Veterinary Technician Medical Records, 2003). The Rock Creek Park veterinary facility functions on a seven-day work week, with staggered schedules for the veterinarians, keepers, and technicians. The clinical staff works from a well-equipped facility that fulfills the recommendations for veterinary facilities outlined by the AAZV (1999). Additionally, the National Zoo employs two veterinarians in the Department of Pathology supported by two laboratory technicians (one technician position currently vacant). Currently the Department of Animal Health has a structured work plan for active case management. Each animal within the hospital is inspected at least twice daily by the veterinary hospital keeper and at least once daily by a veterinarian. Daily rounds are held with the entire hospital staff and often a member of the Pathology Department. During rounds each animal being acutely managed by the hospital is discussed, procedures planned for that day, as well as scheduling for procedures in the future. In addition to daily rounds, the veterinary staff maintains an active case log of both acute cases and chronic cases. This log is updated daily by all veterinarians on clinical service. The veterinary staff meets twice weekly to discuss the management of all cases in the log. In addition to providing medical treatment to injured or ill animals, the Department of Animal Health is mandated by zoo policy and by professional organizations to establish a preventive medicine program (AAZV, 1999; AZA, 2003c). The preventive medicine program at the National Zoo includes quarantine, parasite surveillance procedures and control, immunization, infectious disease screening, and dental prophylaxis (National Zoological Park Preventative Medicine Program, 1998, 1999, 2001, 2003). Strengths and Weaknesses of Veterinary Care at the National Zoo With three full-time veterinarians and two temporary veterinarians, the National Zoo maintains a larger clinical veterinary staff than many other zoos of similar age, size, and animal collection number. For example, the 100-year-old 200-acre Milwaukee County Zoo, with an animal collection of approximately 2,000 representing over 300 species, employs two full-time clinical veterinarians. The Baltimore Zoo, Minnesota Zoological Garden,

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28 ANIMAL CARE AND MANAGEMENT AT THE NATIONAL ZOO: INTERIM REPORT Louisville Zoological Garden, Sedgwick County Zoo, and the Detroit Zoological Garden all with collection sizes and annual budgets similar to those of the National Zoo each employ one or two full-time veterinarians (AZA, 2003b; AAZV, 2004). Approximately 274 veterinarians are employed by the 180 AZA-accredited zoos with on-site veterinary staff (Amand, 2004). Of those veterinarians employed by AZA-accredited zoos, approximately 35 are board certified (by the American College of Zoological Medicine) with six institutions retaining three or more board certified veterinarians: San Diego Zoo, Bronx Zoo (Wildlife Conservation Society), Disney's Animal Kingdom, Saint Louis Zoological Park, North Carolina Zoological Park, and the National Zoo (Amand, 2004). It is important to note that clinical veterinarians at most other zoos also function as the onsite pathologist (performing necropsies, collecting postmortem diagnostic samples, and assigning gross pathologic diagnoses) in addition to their clinical duties, because most zoos do not have full-time veterinary pathologists or a pathology department (Citino, 2000). Unlike most zoo veterinarians, the clinical veterinarians at the National Zoo do not have responsibility for pathology because the National Zoo employs two additional full-time veterinary pathologists in addition to its staff of clinical veterinarians. The San Diego Zoo, Bronx Zoo (Wildlife Conservation Society), Disney's Animal Kingdom, Saint Louis Zoological Park, Philadelphia Zoo, and the National Zoo are among the few institutions with separate pathology departments. Other zoos utilize schools of veterinary medicine or commercial laboratories for pathology needs. To assess the quality of veterinary medical care at the National Zoo, members of the committee met with veterinary staff, keepers, and curators; examined written policies and procedures of the Department of Animal Health; evaluated the medical records of select animals currently in the collection, as well as the medical records of particular animals that were brought to the attention of the committee; reviewed the scientific literature; and gathered information on preventive medicine and animal care from other zoological institutions. This process is ongoing and the committee will continue to gather information for the preparation of its final report. However, the information evaluated during the first six months of the project has revealed serious deficiencies in the preventive medicine program at the National Zoo and isolated incidents of unacceptable veterinary care. To date, the committee has reviewed the majority of the animal deaths at the National Zoo that were brought to the public's and Congress's attention through media coverage. In the committee's opinion, after a review of medical and pathology records, many of these deaths were due to the advanced age of the animals or preexisting conditions and the medical care provided was adequate and in some cases well beyond any reasonable expectation of care. However, the committee did see evidence of a lack of veterinary knowledge regarding the physiology and nutrition of hoofstock (see Box 2-1) and lapses in veterinary care that was provided to an African bush elephant (see Box 2-2). BOX 2-1 Case Study: Grevy's Zebras (Equus grevyi) "Buumba" (Accession #113393), "Shaka" (Accession #113392), and "Arbez" (Accession #113417) Spring 1999 Three zebras brought to the National Zoo were placed in quarantine (NZP, Medical Records, Accession #113393, #113392, and #113417, Grevy's Zebras). May 12, 1999 Shaka and Buumba were released from quarantine to the Cheetah/Elephant area (NZP, Medical Records, Accession #113393 and #113392, Grevy's Zebras). May 17, 1999 Buumba and Shaka examined by the veterinary staff because keepers reported that Buumba had developed a distended abdomen (NZP, Medical Records, Accession #113393 and #113392, Grevy's Zebras). Buumba's diet reduced from 2 pounds of pellets and 2 flakes of hay to 1 pound of pellets and 2 flakes of hay (NZP, Medical Records, Accession #113393, Grevy's Zebras). Shaka's veterinary record does not reflect any change in (NZP, Medical Records, Accession #113392, Grevy's Zebras). June 15, 1999 Arbez was released from quarantine to the Cheetah/Elephant area (NZP, Medical Records, Accession #113417, Grevy's Zebra). Summer 1999 Zebras' diet was increased to 5 pounds of pellets per day and then later reduced to 4 pounds of pellets and 4 flakes of hay (Wells, 2000b), presumably the diet that these animals received in the fall of 1999. Dietary changes were not noted in the medical records and no nutritionist records could be produced for these animals. (continues)

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ANIMAL CARE AND MANAGEMENT 29 BOX 2-1 (continued) October 30, 1999 Keepers reported that Shaka developed a bloated abdomen (NZP, Medical Records, Accession #113392, Grevy's Zebras). Veterinary staff assessed Shaka and ordered a reduction in food intake (NZP, Medical Records, Accession #113392, Grevy's Zebras). November 8, 1999 Zebras' diet reduced to 2 pounds of pellets, and hay cut in half, though there is no indication what the hay consumption was previously or what measurable amount it would then be (NZP, Keeper's Log, Accession #113417and #113392, Grevy's Zebra). Diet reduction occurred for three or four weeks (Nichols and Stevens, undated; Wells, 2000b) Diet reduction was not noted in any of the three animals' medical records, though the keeper logs indicated the veterinary staff was aware of the diet change; and other National Zoo documents also indicated the change was by order of the veterinary staff (Nichols and Stevens, undated; Wells, 2000a). December 1999 Zebras' diet returned to approximately 4 pounds of pellets and 3 flakes of hay per day (Nichols and Stevens, undated; Wells, 2000b). This change is not noted in the keeper logs, veterinary medical records, or curator report. January 31, 2000 Keeper staff observes Buumba lying on the stall floor (NZP, Keeper's Log, Accession # 113393, Grevy's Zebra). Veterinary staff sedate Buumba, examine and administer intravenous fluids and other medications (NZP, Medical Records, Accession #113393, Grevy's Zebra). Buumba recovered from sedation and was then placed into his stall for the night (NZP, Medical Records, Accession #113393, Grevy's Zebra). The keeper logs reflect that veterinary staff also examined Shaka and Arbez, and determined that these animals were overweight (NZP, Medical Records, Accession #113417, #113392, Grevy's Zebras). Shaka's and Arbez's diet were reduced from 4 to 3 pounds of pellets per the veterinarian's orders (NZP, Keeper's Log, Accession #113417 and #113392, Grevy's Zebras). The examination and resulting reduction in diet were not documented in the veterinary medical record of either animal (NZP, Medical Records, Accession #113417 and #113392, Grevy's Zebras). Buumba died during the night of hypothermia, with inanition [starvation] as a contributing factor (NZP, Accession #113393, Grevy's Zebra, Final Pathology Report #2000-0032). February 1, 2000 Shaka and Arbez were evaluated by the nutritionist and determined to be underweight (NZP, Keeper's Logs, Accession #113417 and #113392, Grevy's Zebras). Their diet was substantially increased (NZP, Keeper's Logs, Accession #113417 and #113392, Grevy's Zebras). The examination and diet change of Shaka and Arbez were not documented in the medical record (NZP, Medical Record, Accession #113417 and #113392, Grevy's Zebras). Zebras should be fed a diet containing 12-14 percent crude protein and 37-51 percent neutral detergent fiber (90 percent dry matter) (Lintzernich and Ward, 1997) with daily feed intake of 1.5-3 percent of body weight. Diets are suggested to be constituted of 25-40 percent low fiber pellets and 60-75 percent grass hay (Lintzernich and Ward, 1997). Diets may need to be altered to reflect changing physiological or environmental conditions. While complete documentation of the zebras' intake are not available for analysis, the death of Buumba due to hypothermia and inanition [starvation], and poor body condition of Shaka and Arbez clearly indicate the zebras were not receiving adequate nutrition. Though various internal National Zoo documents (Nichols and Stevens, undated; Wells, 2000b; Wells, 2000a) generated after the animal's death indicated that the keepers, the curator, and the veterinary staff were all aware of the two diet changes that occurred in November and December, none documented the changes completely, if they were documented at all. It is not apparent to what extent the nutritionist was involved in these decisions, since no nutritionist records could be produced for these animals, though there are indications that diet request forms were submitted to the nutritionist (Wells, 2000a). In addition, some keeper logs pertaining to these animals were not archived, while others were improperly archived. (continues)

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30 ANIMAL CARE AND MANAGEMENT AT THE NATIONAL ZOO: INTERIM REPORT BOX 2-1 (continued) Because the reduction in diet for Shaka and Arbez is not reflected in the medical record, it is not apparent what led to the decision of the veterinary staff to reduce the diet of these animals on January 31, 2000. However, the poor condition of the animals upon evaluation by the nutritionist, as well as the inanition, contributed to Buumba's death, reflects an incorrect assessment of Shaka's and Arbez's body condition by the veterinary staff on January 31, 2000. For mammals at the National Zoo body weight is to be monitored monthly under normal conditions, biweekly when diets are changed, and weekly when monitoring health status. Updated body weight information is to be recorded in the daily keeper reports (National Zoological Park, NZP Department of Animal Health Procedures Animal Body Weights, 2003). It is unknown if functioning scales were available for weighing hoofstock at the time of Bumba's death (Wells, 2003b). In addition, it is apparent that substantial changes were made to Buumba's medical record. The committee received copies of the medical record from the Smithsonian's inspector general (printed on March 29, 2000), Dr. Donald Nichols, formerly the associate pathologist at the National Zoo (printed on May 30, 2002), and from the National Zoo (printed on October 2, 2003). On review of the clinical note entries it is apparent that changes were made to the entries logged on April 25, 1999; May 17, 1999; May 27, 1999; June 2, 1999; and February 1, 2000; and that a new entry was created for May 18, 1999. Comparison of the three different copies of the medical record indicates that all of these changes occurred between May 30, 2002, and October 2, 2003. Changes to the medical record, in some cases as much as three years after the entry was originally made, affect the credibility of the information contained in the medical record. Many other details pertaining to the care of the three zebras is a matter of contention among various zoo staff, including whether attempts were made to have the veterinary staff reevaluate the zebras in December and January and whether the curatorial staff was aware and addressing the lack of adequate heat in the building where the zebras were housed (Nichols and Stevens, undated; Wells, 2000b; Wells, 2000a). The committee was not able to address these issues owing to a lack of documentation, however there is ample evidence that poor record keeping, poor veterinary care and decision making, and lack of involvement of the nutritionist contributed to Buumba's death and the poor condition of the other two zebras. BOX 2-2 Case Study: East African Bush Elephant (Loxodonta africana) "Nancy" (Accession #26223) On August 22, 2000, an East African bush elephant named Nancy was euthanatized because of her advanced age, severity of her clinical symptoms, and her poor prognosis. Between 1997 and her death this animal had been diagnosed with osteoarthritis (a functional or structural failure of an entire joint, including the nearby muscles, bone, ligaments) and osteomyelitis (a chronic inflammation of the bone caused by an infection), as well as suffering from multiple episodes of abdominal edema, skin lesions, and mastitis (inflammation of the mammary gland). She had been treated at various times with anti-inflammatory agents (Tylenol, ibuprofen, phenylbutazone) and immunosuppressants (imuran, prednisone), appropriate treatment regimens for the conditions she developed during this time. In 1999 she developed a toe lesion on her right front foot caused by the osteomyelitis. This was treated with localized injections of antibiotics (amikacin and trimethoprin sulfadiazine), with some success at first. However, she began to lose weight and her condition became resistant to treatment. In the month before her death her condition deteriorated and her apparent discomfort worsened as she began to refuse food and medication (NZP, Medical Records, Accession #26223, East African bush Elephant). Upon necropsy it was determined that Nancy suffered from infection with Mycobacterium bovis, a cause of tuberculosis. This caused extensive pneumonia (inflammation in the lungs) involving 60 percent of her lungs (NZP, Accession #26223, East African Bush Elephant, Final Pathology Report #2000-0331). In 1996, two circus elephants died and were found to be infected with tuberculosis. This led to the establishment of the Guidelines for the Control of Tuberculosis in Elephants (The National Tuberculosis Working Group for Zoo & Wildlife Species, 1997; The National Tuberculosis Working Group for Zoo & Wildlife Species, 2000; The National Tuberculosis Working Group for Zoo & Wildlife Species, 2003), which were widely disseminated in January of 1998. These guidelines are considered the standard of care for captive elephants and were subsequently mandated by the USDA in 1998 (63 Fed. Reg. 15826 [April, 1 1998]). Under these guidelines captive elephants are to be tested annually for tuberculosis through the use of trunk washes. This is the only acceptable way to test for tuberculosis in elephants, as skin and blood tests, like those done (continues)

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ANIMAL CARE AND MANAGEMENT 31 BOX 2-2 (continued) in humans, are unreliable (Montali et al., 1998). Trunk washes will detect only active tuberculosis infections (when the animal is contagious to both other animals and humans) and not latent infections (The National Tuberculosis Working Group for Zoo & Wildlife Species, 2003). During the late 1990s, National Zoo veterinarians were deeply involved in the issue of tuberculosis in captive elephants. In fact, from 1999 to 2001 four scientific articles were published by National Zoo veterinarians on the issue (Larsen et al., 2000; Mikota et al., 2000; Mikota et al., 2001; Montali et al., 1998). In the summer of 1997 and the fall of 1998 Nancy was tested for tuberculosis by trunk washes. However, from October 1998 until her death National Zoo staff failed to test Nancy for tuberculosis. In addition, Nancy's medical record contains an entry from February 6, 1999, stating that "tuberculosis or other granulomatous disease can not be ruled out" as the cause of her clinical symptoms. Nancy most likely carried a latent infection of Mycobacterium bovis, that was activated by the immunosuppressant drugs she started receiving in 1998 (NZP, Accession #26223, East African Bush Elephant, Final Pathology Report #2000-0331). It is impossible to determine whether a tuberculosis trunk wash test in 1999 or 2000 would have detected an active tuberculosis infection in Nancy, however the lack of preventive care is evident. Treatments for tuberculosis were published at least as early as 1994 (Mikota et al., 1994) and if tuberculosis testing of Nancy had been done in 1999 and 2000, it is reasonable to expect that her tuberculosis would have been detected and treated, possibly lessening the severity of her clinical symptoms and her apparent discomfort. However, because her advanced age and the progressive worsening of other medical conditions, it is likely that her euthanasia would still have been necessary at some point. Failures in the Preventive Medicine Program A review of zoo documents indicates that the veterinary department has been failing to follow various aspects of the preventive medicine program. There have been numerous examples of failures to follow quarantine procedures and provide appropriate vaccinations, infectious disease testing, and annual examinations. Quarantine Procedures The purpose of quarantine procedures is to prevent the introduction of pathogens to a zoo when a new animal is added to the collection (AAZV, 1999). Depending on the species, these quarantine procedures include fecal, blood, and tuberculin tests; vaccinations; and serology tests for specific pathogens (AAZV, 1999; AZA, 2003c). In reviewing a sample of 26 medical records the committee found six instances from 1999-2001 where veterinary staff failed to document any procedures or tests to which the animals were subjected during quarantine (see Table 2-1), although the quarantine procedures outlined in the National Zoo Preventative Medicine Program were comprehensive and in accordance with recognized standards (AAZV, 1999; AZA, 2003c). In most of the cases listed in Table 2-2, the only information regarding quarantine procedures and tests is a clinical note stating "Released from quarantine" or "Quarantine complete." Because of the lack of appropriate documentation it is impossible to determine whether veterinary staff administered procedures and testing, and thus a portion of the animal's medical history is not available for future assessment. TABLE 2-2 Animals for Which National Zoo Medical Records Failed to Document Quarantine Procedures and Testsa. Year of Arrival at Animal Accession No. National Zoo American bison 113418 1999 American bison 113419 1999 Grevy's zebra 113392 1999 Grevy's zebra 113417 1999 Fishing cat 113526 2000 Mexican wolf 113645 2001 aThe only indication of quarantine procedures noted in the medical record as "Released from quarantine" or "Quarantine complete." SOURCE: NZP, Medical Records, Accession #113418, #113419, #113392, #113417, #113526, and #113645.

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32 ANIMAL CARE AND MANAGEMENT AT THE NATIONAL ZOO: INTERIM REPORT It appears that zoo policies and quarantine procedures may have been violated on several occasions when staff-owned pets were brought onto National Zoo grounds to have tests performed at the Animal Hospital. Staff members of the Department of Pathology have indicated that most tests performed on staff pets were performed as a professional courtesy, with the approval of the head clinical veterinarian and head pathologist; occasional tests were performed to determine whether an infectious disease was present that could be passed from the pet to a zoo collection animal by way of the staff person (Montali, 2003). It is outside the purview of this committee to comment on whether performing laboratory tests on staff pets as a professional courtesy is a legally acceptable practice at the National Zoo. According to the National Zoo's General Memorandum No. 525 (August 8, 2003), "by law, pets, regardless of the species, are not allowed in the National Zoological Park." However, clinical pathology logs indicate that over 80 laboratory tests performed on staff pets, some dated as late at April 10, 2003, were processed by the Pathology Department (Clinical Pathology Log, January 2004), although it is not clear whether the animals were on zoo grounds each time. If staff pets were brought onto National Zoo grounds to perform tests as a professional courtesy, this action represents a potential risk to the zoo collection and a violation of the zoo's own policies and procedures. Vaccination, Infectious Disease Testing, and Annual Examinations Since 1998, there have been numerous examples of failure to provide vaccinations, tuberculosis tests, and annual physical exams. A summary of information depicting poor adherence to the preventive medical program for 16 animals derived from a sample of 26 individual medical records of major animal groups at the National Zoo is provided in Table 2-3. It is possible that veterinary decisions were made not to vaccinate or not to test certain animals based on their current medical status; however, if these decisions were made, they were not documented in the medical record as should have been done. A recent USDA inspection (USDA, 2004b) noted that a majority of small primates had not received their annual preventive care exam as outlined by National Zoo standard operating procedures. The National Zoo has acknowledged that from the spring of 1999 through the fall of 2002 that veterinary staff failed to adhere to their preventive medicine program due to a staffing gap (NZP, Letter to Committee, December 31, 2003). In the case of the East African elephant, failure to administer an annual tuberculosis test resulted in the failure to diagnose an active case of tuberculosis (see Box 2-2). Annual tuberculosis testing was mandated by USDA in 1998 (63 Fed. Reg. 15826). The National Zoo indicated that the tuberculosis testing that should have occurred sometime in the fall of 1999 was delayed until 2000 "due to a heavy load of veterinary care cases and an understaffed veterinary clinical department" (NZP, Fact Sheet--Elephants at the National Zoo, December 2003). It is unacceptable for preventive care to be delayed in this fashion. In particular, this elephant was being seen by a veterinarian on an almost daily basis during the fall of 1999 and had already been trained to submit to a tuberculosis test (NZP, Medical Records, Accession #26223, East African bush Elephant). Guidelines developed by the AAZV (1999) state that the veterinary medical program at a zoo should emphasize disease prevention. If the failure to provide preventive care to the National Zoo's animal collection was caused by a shortage of staff or the inability of the veterinary staff to implement and follow the National Zoo's preventive medicine program, steps should have been taken immediately by senior management to rectify the situation, either by hiring more temporary or permanent veterinary staff, using existing veterinarians on the research staff to alleviate the backlog of preventive medicine procedures (if these veterinarians are suitably licensed to practice veterinary medicine in Washington, D.C.), providing oversight necessary to ensure effectiveness of the preventive medicine program, or by introducing technical and administrative efficiencies or organizational skills training to increase the efficiency of the veterinary staff. The inability of the National Zoo's veterinary staff to provide vaccinations and annual exams because of time or staffing shortages is not a sound scientific or medical reason for varying from the recognized standard of care outlined in the generally accepted standards preventive medicine guidelines. During the past year the Department of Animal Health has taken steps to begin to improve the implementation of the preventive medicine program. However, as of December 29, 2003, not all of the collection had received scheduled examinations, vaccinations, or tests that were indicated in the National Zoo's Preventative Medicine Program (2003). Though veterinary staff members are in the process of updating their preventive medicine program, they have yet to create a document that describes the current vaccinations, tests, and exams that are planned for each species. It is imperative for the National Zoo to take steps to immediately handle the backlog of procedures outlined by the preventive medicine program and to ensure that adequate preventive medicine is provided in the future.

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ANIMAL CARE AND MANAGEMENT 33 TABLE 2-3 Lapses in Preventive Medicine Program at the National Zoo between 1998-2003a AAZV/AZA National Zoo Vaccination and Preventive Medicine Lapses at the National Zood Testing Guidelinesb Program 1998-2003c Primates Rabies vaccination as Annual exam (great Accession #103823 Orangutan warranted apes exam every Failed to receive annual exam in 2001-2002. Tetanus vaccination 2 years) Failed to receive rabies vaccination and TB every 3-5 years Rabies vaccination test in 2001-2003. annually Failed to receive tetanus vaccination in 2002. TB test annually Tetanus vaccination Accession #112236 Sulawesi crested macaque every 7 years Failed to receive annual exam, rabies vaccination, and TB test in 2001. Accession #102167 Orangutan Failed to receive annual exam, rabies vaccination, and TB test in 1999-2000, 2002-2003. Accession #113376 White-fronted marmoset Failed to receive annual exam, rabies vaccination, and TB test in 2000-2002. Canidae Rabies vaccination as Annual exam Accession #111062 Singing dog warranted Rabies vaccination Failed to receive annual exam and canine Canine distemper every 3 years distemper vaccination in 2002. vaccination as Canine distemper warranted vaccination annuallye Felidae Feline panleukopenia Annual exam Accession #108412 Barbary lion and calicivirus Rabies vaccination Failed to receive panleukopenia and vaccination annually every 3 years calicivirus vaccination in 1999-2000, 2003. Rabies vaccination as Panleukopenia and Failed to receive annual exam in 2003. warranted calicivirus vaccination Accession #113526 Fishing cat annuallye Failed to receive panleukopenia and calicivirus vaccination in 2002-2003 Failed to receive annual exam in 2003. Accession #113184 Sumatran tiger Failed to receive panleukopenia and calicivirus vaccination in 1999-2000, 2002, 2003. Failed to receive annual exam in 2003.

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36 ANIMAL CARE AND MANAGEMENT AT THE NATIONAL ZOO: INTERIM REPORT knowledge of nutrient's metabolism is key (Ullrey, 1996). Animals should also be observed to ensure that the diet is consumed (AAZV, 1999); a simple tool to assess the general nutritional status of an animal is to measure food intake (Allen, 1981). An animal may not consume a diet for such reasons as palatability, group aggression, and excess feed. Changes in the animal's physiologic status (growth, lactation, pregnancy, activity) or environmental conditions may necessitate a change in the diet formulation (Clemens, 1985). Diet preparation and feeding should also be monitored to ensure that the diet is prepared and fed according to the instructions. This monitoring, and feedback, provide an evaluation loop to ensure that animals receive appropriate nutrition for health and welfare. Key components of a nutrition program at a zoo are protocols, record keeping, and communication. Nutrition decisions should be made after input from the nutritionist, veterinarian, curator, keeper, and commissary manager for each animal (Dierenfeld, 1987). Comparative Nutrition Comparative nutritionists play a unique role in animal nutrition. They are asked to formulate diets for potentially thousands of species; domestic animal nutritionists often deal with a single species (Ullrey, 1996). In 1987 only five zoos in North America had nutritionists on staff (Stewart, 1987), and today there are fewer than ten AZA-accredited zoos in the United States with a comparative nutritionist for exotic animals (Braun et al., 2003). Greater emphasis is being placed on the relevance of nutrition in the prevention of disease; current veterinary medical curriculum does not allow students sufficient time to gain necessary knowledge and skill in animal nutrition, therefore, nutritionists are needed to provide knowledge in the optimal use of nutrition for animal health (van't Klooster, 1999). A zoo should have a comparative nutritionist either on staff or as a consultant (Stewart, 1987). An animal nutritionist has educational training in nutritional sciences (Dierenfeld, 1987), and those responsible for zoo animal collections should have an advanced degree (M.S or Ph.D.) in (animal) nutrition or an equivalent number of years of experience in management, design, and implementation of a zoo animal nutrition program (Crissey and Fulton, 1994). Zoo nutritionists should routinely evaluate diets fed to animals in the collection for nutritional value (Stewart, 1987), and revise diets according to changing nutritional status. A particular challenge for a comparative nutritionist is the formulation of diets for environmental (heat or cold stress) or physiologic (growth, lactation, gestation, ageing) challenges (Clemens, 1985). Commissary A movement toward centralized commissaries for diet preparation has been slowly occurring at zoos in the United States. A centralized commissary is preferred for several reasons. Records kept in a central location are more easily reviewed by both nutritionist and veterinary staff; monitoring food quality and inventory are thereby better facilitated. Pest control (including rodent and insect contamination of feed, ingredients, and storage facilities) is more efficient when there is only one location to monitor. A centralized commissary allows for efficient use of equipment and staff time and for better tracking and quality control of inventory (NZP, Commissary Review National Zoological Park, May 14-15, 1992). Individual diets or diets for groups of animals are prepared entirely in the commissary so that animal keepers can offer the diet to animals in the form in which the keepers receive it (Braun et al., 2003). To supply foods that help maintain health and reproduction of the animals is the primary goal of a commissary (Crissey et al., 1987). The safety of food for animal diets can be threatened by biological (i.e., bacteria and mold), chemical (e.g., pesticides, heavy metals, sanitizers), and physical (i.e., wire in a bale of hay) factors (Crissey et al., 1987). An important aspect of food storage and diet preparation is the avoidance of ill employees and bacterial contamination resulting from food not being kept in pest-resistant containers (Stewart, 1986). Loss of nutrients due to degradation over time or exposure to certain elements can also compromise the food safety (Crissey et al., 1987). Employee health and well-being in the preparation of diets should also be considered; dust associated with feed, grain, and forages can cause significant respiratory conditions in commissary staff (Aherin, 1986). Commissary management (e.g., proper storage, inventory control, and quality control) plays a vital role in ensuring safety of food in animal diets.

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ANIMAL CARE AND MANAGEMENT 37 Nutrient Analysis and Quality Control A foundation for any successful zoo animal diet is knowledge of feed composition (Dierenfeld, 1996). Animal diets should be routinely analyzed for nutrient adequacy and suitability for each species (AZA, 2003c). Ingredients and nutritionally complete feeds should have periodic nutrient analysis to ensure accuracy of published nutrient values, or to determine those values when none exist (AZA Nutrition Advisory Group, 2001). Digestibility (affected by feed intake, chemical composition, particle size, feed processing, exercise, and age) of feed ingredients (and the entire diet) is important to consider because it is nutrient digested which are utilized by the animal meets its nutritional needs (Fahey, 1981). Because hay (grass or legume) is a significant portion of diets for many herbivores (particularly ruminant and equine animals), its quality is key to diet formulation and animal health. Hay quality varies because of a number of factors: species, maturity and leafiness, harvesting conditions, contamination (by weeds, pesticides, and herbicides) and location (Rohweder, 1986). Digestibility of hay can be measured for ruminants in a digestion trial or in vitro using rumen fermentation techniques (Rohweder, 1981). Digestibility can be estimated from chemical composition of fiber (acid and neutral detergent fiber) (Van Soest et al., 1991) or soluble carbohydrates (neutral- detergent soluble fiber) (Hall et al., 1998). Animal Nutrition at The National Zoo Animal nutrition at the National Zoo is divided into two areas: research and clinical nutrition. The clinical nutrition division was previously in the Animal Programs Department but now resides in the Animal Health Department (see Figure 1-1) and reports directly to the head veterinarian. The research nutrition division is positioned in the Department of Conservation Biology of the CRC (see Figure 1-1) and reports directly to the head of that department. For the past decade the National Zoo has employed two animal nutritionists: one as head of research and one as head of clinical nutrition. Currently the National Zoo employs a person trained in animal behavior as an acting head of clinical nutrition (on a two-year temporary appointment) at Rock Creek Park and a research Ph.D. animal nutritionist with decades of experience with the National Zoo and its animal collection in the Department of Conservation Biology of the CRC. Little direct interaction occurs between the acting head of clinical nutrition and the research nutritionist. After an initial search for a permanent clinical nutrition position which did not yield an acceptable candidate, the National Zoo is now seeking to fill the position at the Rock Creek Park facility with another temporary appointment (Smithsonian Institution Vacancy Announcement Number 04SP-1021). Physical components of the zoo's nutrition program include a commissary and laboratory. The 2003 AZA report (2003a) stated that "despite NZP's history of world-class nutritional research, animal diets at the National Zoo were not well coordinated amongst veterinary, nutrition and animal care staff." Protocols have now been developed for any diet changes which require approval by the curator to evaluate the impact on animal behavior and animal husbandry practices, the veterinarian to evaluate the impact on animal health, and the nutritionist to evaluate the impact on animal nutrient and metabolic needs (NZP, Nutrition and Commissary Operating Protocols, September 2003). Specific hospital diets are formulated to meet the challenged nutritional needs of sick or injured animals as approved by the nutritionist and veterinarian (NZP, Nutrition and Commissary Operating Protocols, September 2003). All food used as enrichment for the animals must be approved by the clinical nutritionist, veterinarian, and curator. An annual evaluation of diets for is to be implemented at the National Zoo. Some diets are to be reviewed seasonally because nutrient needs may change throughout the year. However, these annual (or seasonal) reviews of dietary adequacy have been compromised. Because of a lack of documentation for standard diets or dietary changes (see Chapter 3) the acting head of clinical nutrition has compiled a database based on a variety of records (nutrition, keeper, curatorial, and veterinary). The acting head of clinical nutrition has served as the acting commissary manager for approximately four months (see "Commissary" below). Commissary The National Zoo has a decentralized commissary at the Rock Creek Park facility, with keeper kitchens located on separate sites for many of the animal enclosure areas. The commissary has a manager and four commissary stewards. The commissary manager is responsible for quality control, handling, and storage of all food

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38 ANIMAL CARE AND MANAGEMENT AT THE NATIONAL ZOO: INTERIM REPORT (NZP, Nutrition and Commissary Operating Protocols, September 2003). Commissary stewards maintain the physical inventory of food items in one of four areas. All food orders are prepared and delivered by commissary stewards. Food is delivered during weekdays at the Rock Creek Park facility by commissary staff to the keeper kitchens, where keepers prepare the diets for individual (or groups of) animals; food is delivered weekly to the CRC (NZP, Nutrition and Commissary Operating Protocols, September 2003). The commissary delivers live food to Rock Creek Park animal units upon receipt from vendors; vendors deliver live food for CRC animals directly to the CRC. A designee in each animal unit orders food by preparing a food order sheet and submitting it to the acting head of clinical nutrition and the commissary manager. A 1992 review (NZP, Commissary Review National Zoological Park, May 14-15, 1992) recommended more centralized diet processing to improve nutritional quality and reduce costs. A plan for developing a centralized commissary by 2005 has been drafted (NZP, Proposed Plan to Develop a Centralized Commissary, October 16, 2003). In the fall of 2003 the commissary manager position became vacant when previous manager retired. The acting head of clinical nutrition assumed the duties of commissary manager. This position has recently been filled on a permanent basis with an experienced warehouse manager who has additional experience as an animal nutrition research technician. The acting head of clinical nutrition will train the new commissary manager. Nutrient Analysis and Quality Control A nutrition laboratory (with six to eight rooms) containing nutrition analysis equipment (aligned with the research nutrition division) is available for nutrition analysis but is underused. The acting head of clinical nutrition performs some nutrient analysis in the laboratory; one federally funded laboratory technician is currently used in a research capacity; other laboratory personnel are only available for research activities because they are supported by research grant funds. Some routine nutritional analysis (mainly mineral and vitamin composition) of feed is performed by outside commercial laboratories. According to operating procedures for systematic and routine laboratory analyses (proximate analysis, fiber fractions, and some major and trace minerals), analyses will be performed four times per year (March, June, September, and December) for forages and primary dry feeds; secondary dry feeds and moist feeds twice per year; and tertiary dry feeds once per year (NZP, Nutrition and Commissary Operating Protocols, September 2003). Nutrient composition (proximate analysis, fiber fractions, some major and trace minerals, and some vitamins) for meat-based diets will be analyzed for each shipment. Microbiologic screenings for Salmonella, Campylobacter, and E. coli 0157 will be conducted for meat-based diets and are analyzed for each shipment (NZP, Nutrition and Commissary Operating Protocols, September 2003). Hay (timothy, orchard grass, and alfalfa) is grown at the CRC for many captive herbivores in the National Zoo collection (NZP, Nutrition and Commissary Operating Protocols, September 2003). The harvested hay bales are held off the ground stored in barns at the CRC. The commissary manager is responsible for monitoring the hay supply and coordinating pickups for the Rock Creek Park facility (NZP, Nutrition and Commissary Operating Protocols, September 2003). Hay quality and nutritional composition are analyzed as forages as mentioned in the previous paragraph. Strengths and Weaknesses in Animal Nutrition at the National Zoo The clinical nutrition program at the National Zoo is currently at risk for continued problems. This is because of several factors, including the lack of permanent, qualified, and experienced leadership; limited or no record keeping over the past decade; poor integration of nutrition with overall animal care programs; and the absence of any documented recent analyses or evaluations of the adequacy of the majority of animal diets. These deficiencies have resulted in several problems affecting the well-being of the animals at the National Zoo. For example, in 2000 a zebra at the Rock Creek Park facility died of hypothermia and malnutrition (see Box 2-1 for detailed discussion). More recently, an unannounced inspection by the USDA identified the inappropriate feeding of seasoned baked fish and beef to apes (USDA, 2004b). The nutrition problems seen in primates and in equines at the National Zoo are not limited to the specific incidents cited. A rudimentary analysis of documented current diets of several primate groups and of zebra at the National Zoo indicate that the animals are not being fed according to requirements and recommendations established by the National Research Council (NRC) for wildlife and relevant domestic species (see Tables 2-4 and 2-5) (NRC,

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ANIMAL CARE AND MANAGEMENT 39 1989a; 2003). The NRC recommendations are used by all government agencies with regulatory oversight of animal care and by the feed industry as the standards for animal feeding. For three primate groups at the National Zoo, diets appeared to be deficient or excessive in specific key nutrients that are critical to normal gut function and to overall animal health (e.g., protein, fiber, vitamins and minerals), or food items were inappropriate to the species' digestive physiology (see Table 2-4) (NRC, 2003; Stevens and Hume, 1995). Additionally, great apes (gorillas and orangutans), tamarins, and marmosets at the National Zoo are being fed animal products (i.e., meat and/or eggs, yogurt), which are not appropriate food items for these species, as they are neither carnivorous (meat-eater) or omnivorous (meat and plant eater). Great apes are frugivorous (fruit eater) or herbivorous (plant eater); for example, orangutans consume primarily fruits, and gorillas consume primarily pith, shoots, leaves, and stems of herbs and shrubs in the wild (NRC, 2003). Tamarins are frugivorous, gumivorous, or insectivorous. The inclusion of inappropriate food items in an animal's diet can result in digestive problems for the animal, which directly impacts its health and welfare, and can create situations that require veterinary medical attention. It is not uncommon for diet problems to exist in zoos because most zoos do not employ a nutrition staff as the National Zoo does. It is impossible to know whether the National Zoo diet records used in this rudimentary analysis accurately reflect the diets actually fed or consumed. In addition, published food/feed composition values, rather than analyzed food/feed composition, were used to estimate nutrient composition of the diets. However, the type and magnitude of problems identified in the few diets examined here represent clear examples of deficiencies in the current nutrition program and potential threats to the health and welfare of the animals. TABLE 2-4 Key nutrients found to be deficient or excessive in diets fed to three primate species at the National Zoo.b National Research National Council Nutrient Zoo Dietc Recommendationsd Comments Orangutan (Pongo pygmaeus) NDF (%)e 13 20 Deficient ADF (%)f 4 10 Deficient Calcium (%) 0.5 0.8 Deficient Phosphorus (%) 0.3 0.6 Deficient Lemur (Lemur catta) Protein (%) 14 15-22 Deficient NDF (%) 15 20 Deficient ADF (%) 4 10 Deficient Vitamin E (IU/kg) 10 100 Deficient Calcium (%) 0.7 0.8 Marginal Phosphorus (%) 0.4 0.6 Deficient Tamarin (Leontopithecus spp.) Protein (%) 26 7 Excessive Vitamin D (IU/kg) 15,327 2,400 Excessive aNZP, Diet Record, Accession #31264, #107881, Orangutan; Accession #106955, #106960, #111251, #111277, #112790, #113319, #113453, #113454, #113482, #113483, 113529, #113530, #113550, #113551, #113569, #113570, #113614, #113670, #113804, #113806, #113807, #113808, Tamarin; and Accession #113682, #113683, #113684, #113685, #113686, #113687, #113688, #113689, Lemur. bThe composition of diets fed (obtained from the National Zoological Park Diet Record forms) were compared to published nutrient requirements and feeding recommendations established by the National Research Council (NRC, 2003). cNutrient composition of the fed diet was determined by calculation of amount fed (as documented on the diet form) and with known nutrient composition of individual diet ingredients as published by USDA Nutrient Database for Standard Reference (U.S. Department of Agriculture, Agricultural Research Service. 2002. USDA National Database for Standard Reference, Release 15, Nutrient Data Laboratory Homepage, http: //www.nal.usda/gov/fnic/foodcomp) and feed composition tables published by the NRC (NRC, 2003). dFrom Nutrient Requirements of Nonhuman Primates, Second Revised Edition (NRC, 2003). eNeutral detergent fiber. fAcid detergent fiber.

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40 ANIMAL CARE AND MANAGEMENT AT THE NATIONAL ZOO: INTERIM REPORT TABLE 2-5 Nutrients found to be excessive or deficient in the current winter diet fed to three zebraa at the National Zoo.b National National Research National National Zoo Diet Council Zoo Dietc Zoo Diet (young Recommendationsd Comments (adult (adult growing (adult diet/young (adult diet/young Nutrient male) male) male) growing diet) growing diet) Protein (g/d) 1255 1156 482 536/650 Excessive/ Deficient Magnesium 27 24 10.2 6/5.7 Excessive/ (g/d) Excessive Potassium 144 123 53.2 20/18.7 Excessive/ (g/d) Excessive Calcium (g/d) 85 72 31 16/19 Excessive/ Excessive Phosphorus 40 40 16 11/11 Excessive/ (g/d) Excessive aNZP, Diet Record, Accession #113392, #113417, and #113805, Grevy's Zebra bThe composition of diets fed (National Zoological Park Diet Record form) were compared to published nutrient requirements established by the National Research Council for equines (NRC, 1989a). cNutrient composition of the fed diet was determined by calculation of amount fed (as documented on the diet form) and with known nutrient composition of individual diet ingredients as published in feed composition tables included in the NRC report series on nutrient requirements of animals (NRC, 1989a). dFrom Nutrient Requirements of Horses (NRC, 1989a). The National Zoo is not fully using its nutrition expertise. The zoo has an active nutrition research program (funded mainly through external grants) with a research nutritionist who has a wealth of knowledge and experience in zoo animal nutrition. In the short term (while the zoo seeks a clinical animal nutritionist), the research nutritionist should collaborate with the acting head of clinical nutrition, (who has limited relevant experience) in the formulation of diets for the animal collection. The zoo could benefit from hiring a permanent, qualified, nutritionist (M.S. or Ph.D. in animal nutrition) with years of experience managing a nutrition program and training in zoo animal nutrition, rather than filling the position temporarily. A job description for this position should clearly define educational requirements, reporting structure and areas of responsibility, essential duties, and collaboration with a research nutritionist. Lack of continuity is a concern with temporary placement; with a temporary placement the zoo could employ a nutritionist who spends a short time at the zoo and then moves to another organization when the placement is finished. This could lead to disruption of nutritional services at the zoo and a failure to develop institutional memory. Recently implemented procedures for diet approval (requiring veterinarian, nutritionist, and curator approval) at the National Zoo are appropriate and should help ensure diet adequacy for animals in the collection, but the lack of appropriate expertise and oversight can place the nutritional care of the animal collection at risk. The research nutritionist and the acting head of clinical nutrition should collaborate immediately on completing the centralization of diet formulation records for each species (or individual animal). A schedule for annual (or seasonal, as appropriate) diet evaluations provides an excellent roadmap for routine diet formulation; however, this plan should not be a substitute for dietary evaluation (and reformulation) needed for individual animal needs (e.g., illness, injury, pregnancy, growth). More frequent (rather than only minimal) routine nutrient analysis of feedstocks would be beneficial for diet formulation and evaluation of the animal collection needs. The National Zoo should examine the support needs of the clinical nutrition position and assess the role of the current federally funded nutrition laboratory technician position in the research nutrition division to determine if there are reporting arrangements that would benefit both the research division and the animal collection. The present commissary has the physical capacity needed for a centralized program and is currently underused (NZP, Commissary Review National Zoological Park, May 14-15, 1992). The National Zoo has developed a draft plan to move diet preparation to a centralized commissary (NZP, Proposed Plan to Develop a Centralized Commissary, October 16, 2003), with an initial pilot program scheduled for late 2004. Many specifics for moving to a centralized commissary are contained both in the 1992 commissary report (NZP, Commissary Review National Zoological Park, May 14-15, 1992) and the National Zoo draft commissary plan (NZP, Proposed Plan to Develop a Centralized Commissary, October 16, 2003). This project will lead to more consistency in diet

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ANIMAL CARE AND MANAGEMENT 41 preparation and reduce the time that keepers spend in diet preparation. The zoo should continue this positive step and move toward a centralized commissary by empowering the acting head of clinical nutrition and new commissary manager to finalize the plan and begin implementation during 2004. Because standard operating procedures, record keeping, and communication protocols have only been updated recently (NZP, Nutrition and Commissary Operating Procedures, September 2003), these activities as they relate to animal nutrition program have not yet been fully implemented. It is essential for the clinical nutrition division to follow through on the timely implementation of these programs and for the clinical nutrition division under qualified leadership to be given authority and responsibility for the success of these programs. Because these programs are relatively new (or newly updated), their impacts on animal care are likely just beginning, and ongoing reevaluation of their effectiveness is essential. Integration of the nutrition records with other animal records (e.g., medical, curatorial, keeper) in a comprehensive information management system is discussed in Chapter 3. Findings and Immediate Needs Finding 2: Shortcomings exist in the animal nutrition program. There has been inadequate communication between the nutrition, keeper, and veterinary staffs; poor consultation between the research nutritionist and the acting head of clinical nutrition; and a lack of standardization and regular evaluation of animal diets. Nutrition records are not currently integrated with other record-keeping systems and, despite having adequate facilities for over a decade, the National Zoo is only now beginning to move toward a centralized commissary. Immediate Needs: The National Zoo should immediately use its existing nutrition expertise by increasing coordination and collaboration between the acting head of clinical nutrition and the research nutritionist to address nutritional issues of the animal collection, including diet review, evaluation, and modification. The zoo also should seek a permanent (rather than temporary), qualified experienced person for the role of clinical nutritionist. Centralization of standard diet formulation records and integration of those records with other record-keeping systems for animal care and management at the National Zoo should be completed. An annual schedule for evaluation of diet formulations for each animal or animal group should be developed and implemented. The National Zoo should finalize its draft plan to centralize the commissary and implement it in 2004. ANIMAL WELFARE The National Zoo currently has two Institutional Animal Care and Use Committees (IACUCs), one each for the CRC and the Rock Creek facility. Both are responsible for ensuring that the living collection and research subjects receive humane care and treatment. Each IACUC is responsible for (NZP General Memorandum No. 15, August 8, 2003, September, 2003) inspecting all animal areas and supporting facilities twice a year and submitting inspection reports; investigating and resolving concerns and complaints brought to their attention; reviewing proposals for research using animals at their respective facilities or field sites; recommending to the zoo director changes to National Zoo practices and procedures to correct deficiencies; recommending to the zoo director the suspension of any activity not being conducted in a manner consistent with current policy and procedures. Animals Used in Research Programs The responsibilities of the IACUCs, as pertains to research animals, are also federally mandated through the Public Health Service Policy on the Humane Care and Use of Laboratory Animals (PHS Policy) and the Animal Welfare Act (AWA). The NIH Office of Laboratory Animal Welfare (OLAW) and the U.S. Department of Agriculture (USDA) oversee compliance with the PHS Policy and AWA, respectively.

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42 ANIMAL CARE AND MANAGEMENT AT THE NATIONAL ZOO: INTERIM REPORT Public Health Service Policy on Humane Care and Use of Laboratory Animals Research at the National Zoo that is supported by the Public Health Service (PHS) is subject to PHS Policy, which requires that all institutions receiving PHS support provide a written Animal Welfare Assurance (Assurance), a document that fully describes the institution's program for the care and use of animals in PHS-conducted or supported activities. PHS Policy requires institutions to appoint an Institutional Animal Care and Use Committee (IACUC) to oversee the institution's animal program, facilities, and procedures, including confirming that projects are conducted in accordance with the Guide for the Care and Use of Laboratory Animals (NRC, 1996b). In addition, the IACUC must inspect semiannually all facilities that are used in PHS-funded research, review animal care and use programs, prepare reports of these inspections and reviews, and maintain minutes of the IACUC meetings and records of animal protocols and changes to protocols (PHS Policies IV.C., B., and E.). The Smithsonian Institution maintains one Assurance for all PHS-funded research that occurs within the Smithsonian Institution, including research at the National Zoo. The Smithsonian Institution's Office of Sponsored Projects is responsible for maintaining the Assurance and providing an annual report to the NIH Office of Laboratory Animal Welfare (PHS Policy IV. F.) that outlines changes to National Zoo's facilities or IACUC membership, a notice of the dates of the semiannual inspections, and any serious instances of noncompliance with PHS Policy or deviations from the provisions of the Guide for the Care and Use of Laboratory Animals. Animal Welfare Act The AWA applies to (1) research activities that use warm-blooded vertebrates except birds, rats of the genus Rattus, and mice of the genus Mus and (2) research that is not initiated to improve nutrition, breeding, management, or production efficiency of the animal under study (9 CFR 1.1). When research being performed at a federal institution (such as the National Zoo) is subject to the AWA, the AWA-covered research is subject to review and oversight by an IACUC in a fashion similar to that dictated by PHS Policy. The IACUC is responsible for reporting deficiencies in animal care and use that occur regarding research animals that are subject to the AWA. These deficiencies are to be reported to the head of the federal agency as outlined in 9 CFR 2.37: Each Federal research facility shall establish an Institutional Animal Care and Use Committee which shall have the same composition, duties, and responsibilities required of nonfederal research facilities by Sec 2.31 with the following exceptions: (a) The Committee shall report deficiencies to the head of the Federal agency conducting the research rather than to APHIS; and (b) The head of the Federal agency conducting the research shall be responsible for all corrective action to be taken at the facility and for the granting of all exceptions to inspection protocol. Each Federal research facility shall establish an Institutional Animal Care and Use Committee which shall have the same composition, duties, and responsibilities required of nonfederal research facilities by Sec 2.31 with the following exceptions: Some research at the National Zoo does not fall under the oversight provided by the Animal Welfare Act or PHS Policy. This is because the research pertains to improving the nutrition, breeding, or management of an animal, does not involve an AWA-covered species, or is not funded by the PHS Animal Exhibition Program at the National Zoo The AWA regulates the treatment of animals on exhibition at the National Zoo (7 U.S.C. 2144). The regulations covering the care, facilities, veterinary care, and enrichment that must be provided to animals on exhibit in the United States are described in 9 CFR Section 3. The Animal and Plant Health Inspection Service (APHIS) in

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ANIMAL CARE AND MANAGEMENT 43 the USDA ensures compliance with the AWA by inspecting exhibitors, and in cases where the AWA is violated, using civil penalties and legal action to force compliance (USDA, 2002). While the AWA clearly defines the responsibilities of the National Zoo IACUCs and the Smithsonian Institution as it pertains to oversight and reporting on the care and use of research animals subject to the AWA, the role of the National Zoo IACUCs, the USDA, and the head of the Smithsonian for overseeing the care and use of animals not used for research (i.e., animals on exhibit or used for breeding at the zoo), is not clearly defined. The USDA's current interpretation of the law is that they do not have enforcement authority at the National Zoo (USDA Office of the General Counsel Fax to the National Academies Committee on the Review of the Smithsonian Institution's National Zoological Park, January 13, 2004). Because of a lack of clarity on enforcement authority at federal institutions, in the past USDA has provided only courtesy inspections at the behest of a federal agency, unless a memo of understanding had been entered into with the federal agency to clarify enforcement and inspection issues. Recently, the U.S. House of Representatives Committee on House Administration, the Smithsonian Institution, and USDA have concluded that inspections of the National Zoo should be conducted without notice or consent (Chairman U.S. House of Representatives Committee on House Administration, 2003; USDA, 2004a). This led to the first unannounced APHIS inspection of the National Zoo's Rock Creek facility in January 2004 (APHIS Inspection Report, 2004). A memorandum of understanding between the USDA and the Smithsonian Institution could clarify issues relating to enforcement of the AWA at the National Zoo. Strengths and Weaknesses in Animal Welfare at the National Zoo Public Health Service Policy Since 1998, at least five research projects at the National Zoo that use animals (domestic and exotic cats and zebrafish) have received PHS funding through NIH (NIH Grant Abstracts 3R01HD023853, 3R01RR008769, 5K01RR000135, 1K01RR017310, 5R03HD039430). This requires that the Smithsonian Institution provide a written Assurance acceptable to the NIH Office of Laboratory Animal Welfare, fully describing the National Zoo's program for the care and use of animals in PHS-conducted or supported activities. PHS Policy further requires that once every 12 months, the institution provide a written report to the NIH Office of Laboratory Animal Welfare detailing changes to the institution's program, facilities, and IACUC membership, and the dates of semiannual IACUC evaluations of the program and facilities, and any serious noncompliance with PHS Policy or deviations from the provisions of the Guide for the Care and Use of Laboratory Animals (PHS Policy IV.F.). Based on its review of records from the Smithsonian Institution's Office of Sponsored Projects and the NIH Office of Laboratory Animal Welfare, the committee cannot confirm whether the Smithsonian Institution had a valid Assurance from 1997 to 2000, a time during which PHS-funded research projects utilizing animals were funded and conducted at the National Zoo. Records indicate that on April 11, 2000 the Smithsonian Institution submitted paperwork to the NIH Office of Laboratory Animal Welfare seeking renewal of its Assurance. On February 19, 2004, the committee received a letter from the NIH Office of Laboratory Animal Welfare stating that the office recently located this submission and now considers the Smithsonian's Assurance to be approved for the period between April 11, 2000 and March 31, 2004 (Garnett letter of February 19, 2004). The committee did not have the opportunity to consider the implications of this letter in its interim report because it was received only a few days before the report was finalized. The status of the Smithsonian's Assurance will be examined more fully in the committee's final report. The Smithsonian Institution's Office of Sponsored Projects also has been unable to provide the committee with evidence that the annual reporting requirement (PHS Policy IV.F.) was fulfilled from 1995-2003. Based on the documents provided to the committee, the IACUC at the Rock Creek Park facility has not consistently fulfilled its responsibilities as required by PHS Policy IV.E. Since at least 2000, the IACUC has not conducted semiannual inspections of facilities used in PHS-funded research or documented IACUC activities through minutes (PHS Policy IV.E.). Due to these failures, the committee cannot discern if PHS-funded research at the Rock Creek facility has been or is being conducted in accordance with the provisions laid out in the Guide for the Care and Use of Laboratory Animals (1996), as is required by PHS Policy. These provisions include: avoidance or minimization of pain and distress; appropriate use of sedation, analgesia, and anesthesia; and the consideration of alternatives to animal use and unnecessary duplication of experiments. There is a lack of documentation that appropriate oversight by the National Zoo, the Smithsonian Institution, or the Office of Laboratory Animal Welfare at NIH was being provided to ensure the welfare of animals used in PHS-funded research.

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44 ANIMAL CARE AND MANAGEMENT AT THE NATIONAL ZOO: INTERIM REPORT Animal Welfare Act It is possible that some PHS-funded research at the National Zoo from 1998 to the present (specifically that on domestic and exotic cats) was subject to the AWA. The lack of record keeping by the IACUC at the Rock Creek Park facility, as well as the Smithsonian Institution Office of Sponsored Projects, is such that the committee cannot determine whether research being conducted at the National Zoo is subject to the AWA or whether other research projects not funded by PHS are subject to the AWA. For example, in 2001, a project to study the organization of memory in nonhuman primates was approved by the Rock Creek IACUC (NZP, IACUC Annual Report: Rock Creek Facility, 2001). The project may in fact be subject to the AWA, as it involves an AWA-covered species and it does not involve research to improve nutrition, breeding, management or production efficiency. However, the Rock Creek IACUC meeting minutes from 2001 do not reflect that this project was ever discussed or approved by the IACUC, and the Rock Creek IACUC records do not contain any information describing the research to be performed. There is no documentation to confirm whether the care these research animals received was in accordance with generally accepted standards and possibly the standards outlined by the AWA. Further, the responsibility for identifying AWA-subject research and notifying the USDA that such research is occurring is the responsibility of the federal agency (in this case, the National Zoo and/or the Smithsonian Institution). This, in turn, triggers the Animal Care Regional Office of the USDA to send annual report forms to the National Zoo to track the research (USDA, 1999). Further investigation of ongoing research at the National Zoo is warranted to determine if AWA-subject research is being conducted. Institutional Animal Care and Use Committee Many animal welfare issues at the National Zoo remain unresolved. Because of the failure of the National Zoo and the Smithsonian Institution to provide the committee with sufficient documentation to enable it to ascertain whether the National Zoo is in compliance with PHS policy and the AWA, animal welfare at the National Zoo remains a serious concern of the committee. In addition, the Rock Creek Park IACUC at the National Zoo has not been diligent in establishing its authority and fulfilling its responsibilities. Although not required by any regulation, the National Zoo did have a committee (previously designated the Animal Welfare Committee and most recently called the Rock Creek Park IACUC) tasked with addressing issues pertaining to the welfare of animals on exhibit and research animals not covered by PHS Policy or the AWA. The Rock Creek Park IACUC did not have a clear mandate as to its responsibilities for ensuring the welfare of exhibit animals and research animals not covered by PHS Policy or the AWA, and generally failed to document their activities adequately. For example, in 2002, four research projects involving exhibit animals were approved; approvals were given for these projects on March 5, March 25, and December 19, 2002 (NZP, IACUC Annual Report: Rock Creek Facility, 2002). However, the IACUC meeting minutes for 2002 reflect that a single meeting was held on December 9. The minutes of that meeting do not state that any of these projects were discussed or approved. The Rock Creek Park IACUC also failed to adequately document its oversight of the welfare of exhibit animals not involved in any research effort. For example, the IACUC inspection of Beaver Valley in April 2000 documented numerous deficiencies that required attention and IACUC follow-up (NZP, IACUC Winter Inspection of Beaver Valley, April 19, 2000). These included (1) the grey seal beach required repair and IACUC needed to make sure that the cooling system functioned properly during the summer; (2) the beaver pool heater required repair and IACUC was to follow up before the winter; (3) the IACUC needed to follow up to ensure that the air conditioning unit in the bobcat enclosure was sufficient during the summer; and (4) a rehabilitating bald eagle required a heat source before the next winter, and the IACUC needed to confirm that this occurred. There is no indication in the IACUC minutes of 2000 or the next IACUC inspection of this area (NZP, IACUC Inspection of Elephant House and Beaver Valley, May, 2001) that the IACUC discussed these deficiencies or monitored the progress of their correction. The lack of clarity about how the Rock Creek Park IACUC functioned, its purview, and its performance typifies the lack of consistency seen elsewhere in National Zoo functions. The Rock Creek Park IACUC's oversight of the welfare of exhibit animals appears to have been an "on again, off again" effort, which may have reflected management's failure to embrace its role in promoting and ensuring the welfare of the animals. It is instructive that a response to a request for copies of complaints submitted to the Rock Creek Park IACUC contained the following statements: "Most of the complaints turned out to be caused by differences of opinion or misunderstandings over

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ANIMAL CARE AND MANAGEMENT 45 how animals should be cared for..." IACUC members would respond informally to "smooth the ruffled feathers..." (NZP, Nichols, 2003). It is clear that uncoordinated responses to individual complaints and concerns failed to address the fundamental need to provide an institutional structure that promoted and supported animal welfare. These sorts of intramural conflicts are resolved best through training that provides individual competence, and communication that instills confidence in one's colleagues. Later, in the National Zoo's response (NZP Nichols Memo, October 16, 2003), it is indicated that the Rock Creek Park IACUC did not keep "official records" of complaint investigations because these were informal, and "...turned out to be problems in communications or staff management -- not animal welfare issues." Given the deaths of the Grevy's zebra and the red pandas at the Rock Creek facility, it should be evident that communication and management are animal welfare issues, and an institutional failure to recognize this compromised further the welfare of other animals at the zoo. It appears that the Rock Creek Park IACUC saw its mandate as one of solving conflict between staff members and not of acting as an advocate for the animals. The National Zoo outlined a new IACUC program in September 2003 (General Memorandum 15). This new IACUC program will be evaluated in the National Acadmies' final report. However, as evidenced by the failures of the previous system and lack of formal training of individuals involved in oversight of animal welfare, the current staff at the National Zoo and the Smithsonian do not have the appropriate training to implement and administer this new IACUC program effectively. It is imperative that the individuals responsible for the administration of the new IACUC program and IACUC committee members receive immediate, extensive training in the rules, regulations, and policies associated with overseeing the use of animals in research from an outside authority. Such training is provided by the OLAW/Applied Research Ethics National Association IACUC 101 course, among others. Animal welfare should be a daily concern for every employee at the National Zoo. In several locations in the National Zoo, animal keepers are doing an admirable job in providing high-quality animal care, even with failing facilities. For example, during visits to the National Zoo, committee members observed that the seal lion exhibit was in severe disrepair, although it continued to house several geriatric animals. The keepers in that area worked around the ongoing repairs to provide the sea lions and seals with excellent training, enrichment, and care. Management should take an active role in promoting staff development and training that instill in the staff the skills needed to fulfill the requirements for animal welfare. Additional aspects of formal training programs and the IACUC programs will be considered for the final report. Findings and Immediate Needs Finding 3: There is a lack of documentation that the welfare of animals has been appropriately considered during the development and implementation of research programs and that complaints regarding the welfare of animals on exhibit were appropriately investigated. There also has been a lack of understanding within the National Zoo and the Smithsonian Institution of the requirements of federal regulations and Public Health Service Policy and how to maintain compliance. Immediate Needs: The National Zoo and the Smithsonian Institution should ensure compliance with all elements of the Animal Welfare Act and the Public Health Service Policy. The National Zoo and the Smithsonian Institution should seek outside training and assistance to achieve compliance with regulations and implement procedures meant to ensure the welfare of research and exhibit animals at the National Zoo. OVERARCHING ISSUES National Zoo staff members have expressed a great affection for the animal collection and a strong desire to provide quality care. While these good intentions provide a fertile ground for high-quality care, the information reviewed by the committee and the direct observations of committee members during inspection tours of the zoo revealed a lack of evidence that the administration has embraced its role in providing for animal care and management; this is compounded by a lack of responsibility and accountability at all levels. While there appears to be pockets of excellence in various units and departments, personal responsibility and accountability for animal care and management are not pervasive at the National Zoo. In reviewing the records of animals in the National Zoo collection, it was apparent that there is a longstanding issue with staff failing to abide by National Zoo policy and procedures. In some cases these failures

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46 ANIMAL CARE AND MANAGEMENT AT THE NATIONAL ZOO: INTERIM REPORT endanger the safety of the animal collection. These incidents include the previously described failures to document changes in animal management (see Box 2-1), failures to adhere with quarantine procedures (Finding 1), and failures to comply with animal welfare policies and procedures (Finding 3). The committee found evidence of failures to obtain the appropriate sign-off on euthanasia forms for an orangutan (NZP, Euthanasia Request Form, Accession #100797, Orangutan) and a tree kangaroo (NZP, Euthanasia Request Form, Accession #110974, Tree Kangaroo). Although there is no indication that these failures led to unnecessary suffering, following proper procedures would have clarified the circumstances surrounding the decisions to euthanatize, which in some cases are now clouded by controversy. The committee also found evidence of failures to complete nutrition forms for diet changes (see Box 2-1). Findings and Immediate Needs Finding 4: There has been poor adherence to the National Zoo's own policies and procedures for animal health and welfare. Immediate Needs: All levels of management should be held accountable for ensuring that National Zoo policies and procedures are followed. All zoo staff should take personal responsibility for educating themselves and adhering with the policies and procedures that pertain to their position and duties.