GLOBAL RETROSPECTIVE ANALYSIS OF PATHOLOGICAL FINDINGS IN ZOO-MANAGED GOELDI'S MONKEYS (CALLIMICO GOELDII), 1965-2018.

As part of the collaborative efforts and goals of managing zoo-housed Goeldi's monkeys, or callimicos (Callimico goeldii), a retrospective review of gross and histopathological postmortem examination reports submitted to the International Studbook Coordinator was carried out by veterinary representatives of the Species Survival Plan to investigate disease trends. A total of 1,887 postmortem reports (1965-2018) collected from more than 150 institutions were reviewed. Histologic findings from 862 postmortem reports and primary causes of mortality were compiled to determine the most common findings. Within the study population, 419 individuals (48.6%) were male, 383 (44.4%) female, and the remaining 60 (7%) of undetermined sex. The primary lesion at death in adults was chronic renal disease. The other prevalent lesions included cardiac disease, myelolipomas, enteritis, colitis, and hepatitis. In Great Britain and mainland Europe, Yersinia spp. infection had significantly higher prevalence than in North American callimico populations. Multiple lesions affecting more than one organ system were identified in many animals of this study population. Results also showed that for adult callimicos in zoological institutions in North America, Europe, and Great Britain, life span has been increasing over the last 50 yr.

After short interbirth intervals, captive callitrichine monkeys have higher infant mortality.

Life history theory predicts a trade-off between the quantity and quality of offspring. Short interbirth intervals-the time between successive births-may increase the quantity of offspring but harm offspring quality. In contrast, long interbirth intervals may bolster offspring quality while reducing overall reproductive output. Further research is needed to determine whether this relationship holds among primates, which have intensive parental investment. Using Cox proportional hazards models, we examined the effects of interbirth intervals (short, normal, or long) on infant survivorship using a large demographic dataset (n = 15,852) of captive callitrichine monkeys (marmosets, tamarins, and lion tamarins). In seven of the nine species studied, infants born after short interbirth intervals had significantly higher risks of mortality than infants born after longer interbirth intervals. These results suggest that reproduction in callitrichine primates may be limited by physiologic constraints, such that short birth spacing drives higher infant mortality.

A comparative study of litter size and sex composition in a large dataset of callitrichine monkeys.

In many birds and mammals, the size and sex composition of litters can have important downstream effects for individual offspring. Primates are model organisms for questions of cooperation and conflict, but the factors shaping interactions among same-age siblings have been less-studied in primates because most species bear single young. However, callitrichines (marmosets, tamarins, and lion tamarins) frequently bear litters of two or more, thereby providing the opportunity to ask whether variation in the size and sex composition of litters affects development, survival, and reproduction. To investigate these questions, we compiled a large dataset of nine species of callitrichines (n = 27,080 individuals; Callithrix geoffroyi, Callithrix jacchus, Cebuella pygmaea, Saguinus imperator, Saguinus oedipus, Leontopithecus chrysomelas, Leontopithecus chrysopygus, Leontopithecus rosalia, and Callimico goeldii) from zoo and laboratory populations spanning 80 years (1938-2018). Through this comparative approach, we found several lines of evidence that litter size and sex composition may impact fitness. Singletons have higher survivorship than litter-born peers and they significantly outperform litter-born individuals on two measures of reproductive performance. Further, for some species, individuals born in a mixed-sex litter outperform isosexually-born individuals (i.e., those born in all-male or all-female litters), suggesting that same-sex competition may limit reproductive performance. We also document several interesting demographic trends. All but one species (C. pygmaea) has a male-biased birth sex ratio with higher survivorship from birth to sexual maturity among females (although this was significant in only two species). Isosexual litters occurred at the expected frequency (with one exception: C. pygmaea), unlike other animals, where isosexual litters are typically overrepresented. Taken together, our results indicate a modest negative effect of same-age sibling competition on reproductive output in captive callitrichines. This study also serves to illustrate the value of zoo and laboratory records for biological inquiry.

COMPARISON OF TRANSCUTANEOUS ULTRASOUND AND COMPUTED TOMOGRAPHY EVALUATION OF KIDNEY SIZE AND EVALUATION OF ADRENAL GLAND SIZE USING ULTRASOUND IN A COLONY OF CALLIMICOS ( CALLIMICO GOELDII).

Both kidney and adrenal gland disease have been identified in callimicos ( Callimico goeldii). Ultrasonography (US) and computed tomography (CT) are routinely utilized in veterinary patients with suspected renal or adrenal disease to determine size, shape, and echogenicity of these organs. No previous US and CT kidney and adrenal gland measurements have been published for callimicos. In this study, 14 callimicos were anesthetized using isoflurane via facemask to evaluate kidney and adrenal gland size using US for both organs and CT for kidneys. Animals were considered clinically healthy based on history, physical examination, hematology, serum chemistry, urinalysis, and abdominal US. Ultrasound organ measurements for length (L), width (W), and height (H) in centimeters (mean/median, 95% confidence interval) in clinically healthy animals were right kidney (L = 1.90, 1.76-2.01; W = 1.05, 0.97-1.13; H = 1.59, 1.48-1.69), left kidney (L = 1.84, 1.72-1.95; W = 1.16, 1.04-1.28; H = 1.54, 1.43-1.65), right adrenal gland (L = 0.38, 0.33-0.57; H = 0.19, 0.15-0.31) and left adrenal gland (L = 0.36, 0.32-0.39; H = 0.18, 0.17-0.20). All kidney measurements were positively correlated with animal weight ( P < 0.05) but had no significant correlation to age. Measurements did not have any significant relationship to evaluated blood and urine parameters. Results from this study establish baseline measurements for callimico kidneys and adrenal glands to help clinicians use these imaging modalities for evaluation of these organs in this endangered species.

EVALUATION OF IN-HOUSE URINE DIPSTICK, REFERENCE LABORATORY URINALYSIS, AND URINE PROTEIN: CREATININE RATIO FROM A COLONY OF CALLIMICOS (CALLIMICO GOELDII).

This study evaluated results from an in-house (IH) laboratory dipstick, a reference laboratory (RL) urinalysis, and urine protein : creatinine (UPC) ratios from callimicos ( Callimico goeldii ). Urine was collected from 25 individuals comprising a single colony under professional care in North America and compared based on laboratory, sex, age class, and presence or absence of a normal urinalysis. Urine specific gravity and pH between laboratories were statistically different. Overall, 56% to 100% of animals had at least a trace amount of protein in their urine. In comparing normal and abnormal urinalyses, IH dipstick protein, RL dipstick protein, RL pH, quantitative protein measurement, and UPC ratios were all statistically different. Eleven animals (44%) had UPC ratios that were ≥0.5. Based on results of this study, UPC > 0.3 was found to be abnormal and supportive of renal compromise in callimicos. Higher protein concentrations on the IH dipstick, the quantitative protein concentration, and UPC ratio in the 1- to 4-yr-old age class were the only significant age-related differences. There was no association between any categorical variable (glucose, blood, bilirubin, ketones, urobilinogen) and abnormal urinalysis. There were no differences between sexes. Since renal disease is a major cause of morbidity and mortality in this species, the authors recommend including routine urinalyses and UPC ratios as part of preventive care programs for callimicos. These data provide the first published information on urinalysis and UPC ratios in callimicos and will serve as a helpful reference for interpreting results and evaluating patients with renal disease.

RETROSPECTIVE REVIEW OF THE PREVALENCE OF MYELOLIPOMA IN GOELDI'S MONKEYS (CALLIMICO GOELDII).

Myelolipomas are mesenchymal tumors composed of adipose and hematopoietic tissue. They have been reported in many species, including domestic dogs and cats, birds, mustelids, wild felids, and nonhuman primates. Myelolipomas in Callitrichidae have been reported at postmortem examination and rarely antemortem. Multiple cases of hepatic myelolipomas associated with morbidity in Chicago Zoological Society's collection of Goeldi's monkeys (Callimico goeldii) prompted a global retrospective study to determine the prevalence and investigate factors associated with this condition. A total of 842 postmortem examination reports (1965-2013) collected from 133 captive collections were reviewed. Myelolipomas were reported in 17.2% (n=145) of animals, with significantly more female cases than male (P=0.023). There was a significantly older mean age at death in affected animals (134 months) compared to unaffected animals (79 months) (P<0.0001). Myelolipomas were diagnosed in the liver in all affected animals, and rarely in the adrenal or spleen. One in five (22.1%) affected Callimico had notable morbidity associated with this disease, which is markedly different from the primarily benign reports in other species. To identify disease, prevent morbidity from hepatic myelolipoma, and improve care of Callimico species in zoological collections, new Species Survival Plan (SSP) medical management recommendations include incorporating abdominal ultrasonographic examination during routine physical examinations in addition to previously recommended hematological and serum biochemical evaluations. Future studies are merited to examine the prevalence, risk factors, health effects, and treatment options of myelolipoma in living collections.

Life span, reproductive output, and reproductive opportunity in captive Goeldi's monkeys (Callimico goeldii).

In the absence of long-term field studies, demographic and reproductive records from animals housed in zoos and research laboratories are a valuable tool for the study of life history variables relating to reproduction. In this study, we analyzed studbook records of more than 2,000 individuals born over a 40-year period (1965-2004) to describe life history patterns of captive Goeldi's monkeys (Callimico goeldii) housed in North America and Europe. Using Kaplan-Meier survival analysis methods, we found the mean life span to be 5.5 years. The rate of infant mortality, defined as death before 30 days, was approximately 30%, with European animals being more likely to survive infancy than North American animals. When individuals surviving at least 1.5 years are considered, lifetime reproductive output averaged 3.5 offspring, yet more than one-third of individuals did not produce any offspring. Using a smaller dataset of individuals with known pairing histories, we developed a measure of opportunity for reproduction (OFR), which represented the total time an individual was known to be housed with a potential mate. For both sexes, we found that the correlation between OFR and number of offspring produced was much higher than the correlation between life span and number of offspring produced. This result highlights the importance of taking into account an individual's OFR. As a whole, our findings help characterize the life histories of captive Goeldi's monkeys and emphasize the impact management practices may have on reproductive success.

Fatal disseminated encephalitozoonosis in a captive, adult Goeldi's monkey (Callimico goeldii) and subsequent serosurvey of the exposed conspecifics.

A captive, adult male Goeldi's monkey (Callimico goeldii) (GM) presented in acute respiratory distress 4 yr after importation into the United States from Europe. Radiographs and echocardiogram were consistent with heart failure. The monkey died within 24 hr of presentation. Necropsy findings included multicentric arteritis and aortitis with aneurysm associated with microsporidian organisms morphologically consistent with Encephalitozoon species. Polymerase chain reaction confirmed organisms were Encephalitozoon cuniculi. Sequence analysis of amplicons generated by using primers specific for the polar tube protein of E. cuniculi determined the organism to be genotype II. An E. cuniculi serosurvey of potentially exposed conspecifics that represented approximately 40% of the captive GM population in the United States was conducted. Multiple individuals that had been imported from Europe with the individual of this report were seropositive via an immunofluorescent antibody assay for E. cuniculi. Multiple samples were available from 3 individuals that demonstrated a decrease in titer or reversion to seronegative status within 3 yr of initial positive status. All other GM were negative on serology. This case is unique in that the genotype identified (genotype II) was different than the genotype (genotype III) reported in other New World primate (NWP) species, the patterns of arteritis were different from the typical pattern of microsporidial vasculitis described in other species, and clinical disease was observed in an adult. Most reported cases of clinical disease secondary to E. cuniculi in NWP have been in neonates and juveniles.