Can we eliminate the primate pet trade in the United States?

International laws and conventions have gone a long way in reducing the number of wild primates entering the United States of America (US) for the pet trade. However, breeding primates for sale to private owners in the United States continues, and individual states present a bewildering array of laws and regulations on the holding of primates as pets. As primatologists we can act to decrease the demand for primate pets by (1) speaking out on the inappropriate use of primates in mass media and especially in social media; (2) not posing in photographs in close proximity to primates; (3) continuing to educate about why primates do not make good pets; and (4) contributing to the science that underlies state and federal legislation with the goal of eliminating captive breeding of primates for the pet trade. We encourage primatologists and others in related fields to be cognizant of the persistent commercialization of primates and be willing to take action to deter it.

Assessing the genetic composition of cotton-top tamarins (Saguinus oedipus) before sweeping anthropogenic impact.

During the last century, the critically endangered cotton-top tamarin (Saguinus oedipus) has been threatened by multiple anthropogenic factors that drastically affected their habitat and population size. As the genetic impact of these pressures is largely unknown, this study aimed to establish a genetic baseline with the use of temporal sampling to determine the genetic makeup before detrimental anthropogenic impact. Genomes were resequenced from a combination of historical museum samples and modern wild samples at low-medium coverage, to unravel how the cotton-top tamarin population structure and genomic diversity may have changed during this period. Our data suggest two populations can be differentiated, probably separated historically by the mountain ranges of the Paramillo Massif in Colombia. Although this population structure persists in the current populations, modern samples exhibit genomic signals consistent with recent inbreeding, such as long runs of homozygosity and a reduction in genome-wide heterozygosity especially in the greater northeast population. This loss is likely the consequence of the population reduction following the mass exportation of cotton-top tamarins for biomedical research in the 1960s, coupled with the habitat loss this species continues to experience. However, current populations have not experienced an increase in genetic load. We propose that the historical genetic baseline established in this study can be used to provide insight into alteration in the modern population influenced by a drastic reduction in population size as well as providing background information to be used for future conservation decision-making for the species.

Proyecto Titi: Teaching children that cotton-top tamarins (Saguinus oedipus) are not appropriate pets.

Cotton-top tamarins (Saguinus oedipus) are a critically endangered species found only in Colombia. Their survival is threatened by extensive habitat destruction and the illegal pet trade. Because many people in Colombia have a low level of awareness of cotton-top tamarins and even less understanding of the impacts that the illegal pet trade has on the species and its long-term survival, Proyecto Tití has developed a series of programs for children in rural elementary schools that introduce children to cotton-top tamarins. This study examines Proyecto Titi's efforts to reduce the desire to have a cotton-top tamarin as a pet with outcomes focused specifically on (1) creating an emotional connection between people and cotton-top tamarins, (2) identifying the feelings and understanding the challenges that cotton-top tamarin face when they are kept as pets, and (3) empowering students to make positive choices to help cotton-top tamarins. Both TITI KIDS and TITIRITIANDO programs helped students to (1) increase their knowledge of cotton-top tamarins, (2) understand the damage that the pet trade has on individual animals and the long-term survival of cotton-top tamarins and (3) provide practical actions that they can engage in to protect cotton-top tamarins for the future. Our hope is that students from our programs become advocates for conservation in their communities and assist in the long-term conservation activities to protect cotton-top tamarins in Colombia.

Vascular, cardiac, and renal lesions attributed to primary systemic hypertension in western pygmy marmosets (Cebuella pygmaea).

In a retrospective study of a western pygmy marmoset (Cebuella pygmaea) colony, postmortem examination of 1/8 juvenile and 29/47 adult animals identified vascular, cardiac, and renal lesions consistent with systemic hypertension. This included frequent renal arteriolar hypertrophy, hyaline and proliferative arteriolosclerosis, fibrinoid necrosis of arterioles, glomerulosclerosis, and nephrosclerosis. Affected animals ranged from 0.6 to 12 years of age (mean 6 years) and had an observed male predominance. Genealogical relatedness was evident in several breeding pairs and spanned multiple generations. Concurrent cardiac and renal disease was commonly identified, although frequently subclinical, and both were important causes of morbidity and mortality in affected animals. Cardiomegaly and hypertrophy were typical features and were accompanied by left atrial thrombosis in 10 animals. Signs of heart failure included chronic pulmonary edema in 20 cases and body cavity effusions in 17. In the kidneys, 19 cases had glomerular disease and hypertensive vasculopathy, and 26 cases had nephrosclerosis or glomerulosclerosis. Common extrarenal secondary causes of hypertension were excluded by necropsy examination. The pathogenesis is suggested to involve primary hypertension leading to renal and cardiac disease. Elevated sympathetic activity might be an underlying factor in the frequent development of primary systemic hypertension in the pygmy marmoset, as for the owl monkey.

Seasonality of reproduction in wild cotton-top tamarins (Saguinus oedipus) in Colombia.

Seasonal availability of resources can influence the timing and success of reproduction in primates. This study examines the annual pattern of conceptions, mid-term (13 weeks) and full-term (26 weeks) pregnancy losses, births, and infant survivorship of the Critically Endangered cotton-top tamarin (Saguinus oedipus) at Proyecto Tití's long-term field site in Santa Catalina, Colombia. Using 18 years of behavior, physical exam, and fecal steroid data (N = 51 females, 168 conceptions, 121 liters), fecal estrone conjugate (E1 C) and pregnanediol-3-glucuronide (PdG) or progesterone (P4) profiles were examined to investigate the relationships between female reproductive patterns and reproductive success with feeding and climatic data. Cotton-top tamarins demonstrated seasonal patterns of reproduction and pregnancy losses. We found positive correlations between peak conception and nectarivory, births and rainfall, and mid-lactation and frugivory. High body mass mothers reproducing during the peak season were more likely to have infants survive. Overall, these results suggest that tamarins use a "relaxed income-breeder" strategy. Cotton-top tamarins appear to maximize reproductive output at the time of ovulation, and can reduce their investment in the current reproductive effort at many stages. Changes in food availability due to habitat loss and climate change will require the Critically Endangered cotton-top tamarins to alter their reproductive strategies to survive.

Factors influencing the survival of wild cotton-top tamarin (Saguinus oedipus) infants.

Studies of cooperative breeding species have suggested that helpers are needed for infant survival and that helpers gain skills to successfully raise their own offspring. Studies of callitrichids in managed care and early field studies suggested that group size correlated with infant survival and that helpers needed to learn parental skills to be successful breeders. We present infant survival data from a 20-year field study of cotton-top tamarins (Saguinus oedipus) in Colombia involving 126 litters born to 41 females. There was no difference in the survival of male and female offspring to 6 months of age. However, litter size impacted survival, with triplet litters having lower survival and male triplets having lower survival than females. Loss of infants was highest in the first week of life and, of the animals remaining in the group at 6 months of age, 90% of them survived to 1 year. The mean length of time in the natal group was 2.3 years but some young migrated to other groups after 4 months of age. Group size and number of male helpers (>1 year) was not related to infant survival. However, groups with only one male had fewer surviving infants. Primiparous females had lower infant survival, but previous infant care experience by mothers as helpers had no effect on survival. A major cause of infant loss was group disruption due to deaths/evictions/loss of the reproductively active animals, or immigration of pregnant females. Thus, factors that cause a change in the stability of the reproductively active animals can disrupt group cohesion. Capture of individuals for the illegal pet trade, as well as habitat fragmentation, may increase competition between groups for access to territories and breeding opportunities. This may have long-term impacts to infant survival in this critically endangered species.

A modified diet to support conservation of the Atala hairstreak butterfly (Eumaeus atala Poey).

Raising insects in a laboratory for release into the wild is a common conservation practice, but maintaining breeding colonies year-round can be limited by seasonal food availability. Food availability is particularly challenging for insects which depend on specific host plants. For example, our early efforts to rear the imperiled Atala hairstreak butterfly (Eumaeus atala Poey) resulted in colony failure during winter due to lack of food. To overcome this barrier, we developed a modified freeze-dried host plant diet to support the colony. The diet consisted of reconstituted freeze-dried leaves and stems from fresh-growth coontie (Zamia integrifolia), the host plant for the Atala butterflies. We fed larvae less than 9 mm on this freeze-dried diet and transferred them to live coontie plants after they were more than 9 mm. We reared a colony of Atala butterflies using these methods for 859 days, resulting in more than 3400 animals released into the wild. Comparing colony counts during that time period to the 548 days we reared them without modified freeze-dried diet showed a clear benefit in using freeze-dried diet. A growth trial (N = 40) of larvae fed on only freeze-dried diet compared to larvae fed on fresh coontie cuttings found no significant difference in larval or pupal development between groups (p = 0.71 and p = 0.47, respectively). We, therefore, conclude that the freeze-dried diet provided an appropriate alternative for Atala colonies when fresh growth from the host plant is unavailable, and we recommend use of this technique for raising other host plant-dependent insect species of conservation concern.

Mission impossible or mission accomplished: Do zoo organizational missions influence conservation practices?

Conservation is an important organizational focus for zoos and aquariums. Organizational identity theory predicts a relationship between what is central to organizations, such as their mission statements, and their strategic activities. Based on this theory, we tested how organizational missions relate to their conservation strategies and practices. Tax forms and websites provided data from 173 zoos and 38 aquariums in the Association of Zoos and Aquariums in North America. We analyzed conservation mission strength, organizational characteristics, and project features with dependent variables representing the depth of organizational conservation commitments: amount of grants zoos funded, number of partner organizations, and number of projects per zoo. On tax forms, the average amount of total conservation grants donated to partner organizations per zoo was over $650,000, while the average number of partners reported on the tax forms was two. The content analysis of websites revealed an average of 14 conservation partners and 10 projects per zoo. Negative binomial regression models were significant. The financial analysis revealed that only the number of zoo personnel, as a surrogate for organization size, significantly predicted the amount of zoos' conservation grants. Website analyses found increasing budgets, organizational involvement, and geographic reach of the projects predicted increasing numbers of conservation projects and partnerships. However, our findings did not support the hypothesized relationship-strength of organizational mission did not predict strategy and activities. Zoos could do more to strategically activate their organizational identities and conservation missions to achieve their conservation goals.

Identifying prognostic structural features in tissue sections of colon cancer patients using point pattern analysis.

Diagnosis and prognosis of cancer are informed by the architecture inherent in cancer patient tissue sections. This architecture is typically identified by pathologists, yet advances in computational image analysis facilitate quantitative assessment of this structure. In this article, we develop a spatial point process approach to describe patterns in cell distribution within tissue samples taken from colorectal cancer (CRC) patients. In particular, our approach is centered on the Palm intensity function. This leads to taking an approximate-likelihood technique in fitting point processes models. We consider two Neyman-Scott point processes and a void process, fitting these point process models to the CRC patient data. We find that the parameter estimates of these models may be used to quantify the spatial arrangement of cells. Importantly, we observe characteristic differences in the spatial arrangement of cells between patients who died from CRC and those alive at follow up.

A comparison of penetration and damage caused by different types of arrowheads on loose and tight fit clothing.

Bows and arrows are used more for recreation, sport and hunting in the Western world and tend not to be as popular a weapon as firearms or knives. Yet there are still injuries and fatalities caused by these low-velocity weapons due to their availability to the public and that a licence is not required to own them. This study aimed to highlight the penetration capabilities of aluminium arrows into soft tissue and bones in the presence of clothing. Further from that, how the type and fit of clothing as well as arrowhead type contribute to penetration capacity. In this study ballistic gelatine blocks (non-clothed and loose fit or tight fit clothed) were shot using a 24lb weight draw recurve bow and aluminium arrows accompanied by four different arrowheads (bullet, judo, blunt and broadhead). The penetration capability of aluminium arrows was examined, and the depth of penetration was found to be dependent on the type of arrowhead used as well as by the type and fit or lack thereof of the clothing covering the block. Loose fit clothing reduced penetration with half of the samples, reducing penetration capacity by percentages between 0% and 98.33%, at a range of 10m. While the remaining half of the samples covered with tight clothing led to reductions in penetration of between 14.06% and 94.12%. The damage to the clothing and the gelatine (puncturing, cutting and tearing) was affected by the shape of the arrowhead, with the least damaged caused by the blunt arrowheads and the most by the broadhead arrows. Clothing fibres were also at times found within the projectile tract within the gelatine showing potential for subsequent infection of an individual with an arrow wound. Ribs, femur bones and spinal columns encased in some of the gelatine blocks all showed varying levels of damage, with the most and obvious damage being exhibited by the ribs and spinal column. The information gleaned from the damage to clothing, gelatine blocks and bones could potentially be useful for forensic investigators, for example, when a body has been discovered with no weapons or gunshot residue present.

Ecological Causes and Consequences of Intratropical Migration in Temperate-Breeding Migratory Birds.

New discoveries from direct tracking of temperate-breeding passerines show that intratropical migration (ITM) occurs in a growing number of species, which has important implications for understanding their evolution of migration, population dynamics, and conservation needs. Our large sample size ([Formula: see text]) for purple martins (Progne subis subis) tracked with geolocators to winter sites in Brazil, combined with geolocator deployments at breeding colonies across North America, allowed us to test hypotheses for ITM, something which has not yet been possible to do for other species. ITM in purple martins was not obligate; only 44% of individuals exhibited ITM, and movements were not coordinated in time or space. We found no evidence to support the resource hypothesis; rainfall and temperature experienced by individual birds during their last 2 weeks at their first roost site were similar to conditions at their second roost site after ITM. Birds generally migrated away from the heavily forested northwestern Amazon to less forested regions to the south and east. ITM in this aerial insectivore appears to support the competition-avoidance hypothesis and may be triggered by increasing local density in the core wintering region. Full life cycle models and migratory networks will need to incorporate ITM to properly address seasonal carryover effects and identify which wintering regions are most important for conservation.

The vocal repertoire of the Key Largo woodrat (Neotoma floridana smalli).

The Key Largo woodrat (Neotoma floridana smalli) is an endangered rodent endemic to the island of Key Largo, FL. There is little information on vocal communication in this species and descriptions of the acoustic structure of calls are lacking. A captive breeding program was established as part of the recovery plan for the species, providing the opportunity to investigate the vocal repertoire and acoustic structure of calls in both wild and captive contexts. Audio and video recordings were conducted at the Crocodile Lake National Wildlife Refuge in Key Largo and at Disney's Animal Kingdom(®). Analysis of the acoustic structure of calls resulted in four provisional call types: "Tonal calls" consisted of "ultrasonic vocalizations" (40 kHz fundamental frequency, F(0)), "high squeaks" (10 kHz F(0)), and "squeaks" (1.8 kHz F(0)). "Noisy," broadband calls known as "raspy" vocalizations did not exhibit fundamental frequencies, but contained several prominent spectral peaks (from 9 to 40 kHz). The social contexts of vocal production showed that all four call types were associated with pup need or interactions between pups and dams, and that raspy vocalizations were associated with courtship and copulation. Adults without pups exhibited little or no vocal activity, which may result from solitary lifestyles and predator avoidance.

Nonhuman Primate Paternal Care: Species and Individual Differences in Behavior and Mechanisms.

Direct care of offspring by the father (sire) is relatively rare in primates. Besides humans, there are a number of species where the male is essential for the survival of offspring: marmosets, tamarins, titis and owl monkeys, some lemurs, and siamangs. All these species show reduced sexual dimorphism, territoriality, and biparental care. However, timing and levels of direct care may vary among these species. Here, relying on both lab and field data, we address the variability found in father's involvement with his infants, the behavioral, neuroendocrine and sensory systems that are a cause and consequence of paternal care, and social bonds between the breeding pair. We integrate studies of laboratory animals (where detailed observations and experimentation are possible) with field studies (which illuminate the ecological and evolutionary functions of paternal care) and discuss the future directions for examining the proximate and ultimate mechanisms of paternal care in nonhuman primates.

Measuring positive and negative affect in the voiced sounds of African elephants (Loxodonta africana).

As in other mammals, there is evidence that the African elephant voice reflects affect intensity, but it is less clear if positive and negative affective states are differentially reflected in the voice. An acoustic comparison was made between African elephant "rumble" vocalizations produced in negative social contexts (dominance interactions), neutral social contexts (minimal social activity), and positive social contexts (affiliative interactions) by four adult females housed at Disney's Animal Kingdom®. Rumbles produced in the negative social context exhibited higher and more variable fundamental frequencies (F(0)) and amplitudes, longer durations, increased voice roughness, and higher first formant locations (F1), compared to the neutral social context. Rumbles produced in the positive social context exhibited similar shifts in most variables (F(0 )variation, amplitude, amplitude variation, duration, and F1), but the magnitude of response was generally less than that observed in the negative context. Voice roughness and F(0) observed in the positive social context remained similar to that observed in the neutral context. These results are most consistent with the vocal expression of affect intensity, in which the negative social context elicited higher intensity levels than the positive context, but differential vocal expression of positive and negative affect cannot be ruled out.

Development of husbandry practices for the captive breeding of Key Largo woodrats (Neotoma floridana smalli).

The Key Largo woodrat is an endangered rodent endemic to the island of Key Largo in the Florida Keys. After several reports documented a steep decline in the population, the US Fish and Wildlife Service developed a recovery plan, including captive breeding and reintroduction. Captive breeding efforts were to be focused on providing animals for future reintroduction to protected areas on Key Largo. However, little was known about the husbandry needs or reproductive behavior of this elusive nocturnal species. In 2005, Disney's Animal Kingdom(®) received 11 animals and began to systematically investigate methods of breeding Key Largo woodrats. Since the program's inception, 30 pups have been born and successfully parent reared. In this report, we describe some of the husbandry techniques that have contributed to the success of the Key Largo woodrat captive breeding program at Disney's Animal Kingdom(®) . The results obtained may be of use to other facilities maintaining woodrats and other rodent species.

GPS assessment of the use of exhibit space and resources by African elephants (Loxodonta africana).

In public discussions of animal rights and welfare, we as members and proponents of zoological institutions often face significant challenges addressing the concerns of our detractors due to an unfortunate deficiency in systematically collected and published data on the animals in our collections. In the case of elephants, there has been a paucity of information describing their use of space within captive environments. Here, using collar-mounted GPS recording devices, we documented the use of exhibit space and resources by a herd of five adult female African elephants (Loxodonta africana) housed at Disney's Animal Kingdom((R)). We found that dominant animals within the herd used a greater percentage of the available space and subordinate females avoided narrow or enclosed regions of the enclosure that we termed "restricted flow areas." In their use of other resources, dominant females demonstrated increased occupation of the watering hole over subordinate females, but all females demonstrated relatively equivalent use of the mud wallow. Overall, our results provide preliminary evidence that position within the dominancy hierarchy impacts the percentage of space occupied in a captive setting and may contribute to resource accessibility. These findings can be applied to future decisions on exhibit design and resource distribution for this species.

Preliminary investigation into the use of Micro-CT scanning on impact damage to fabric, tissue and bone caused by both round and flat nosed bullets.

Firearm offences in the UK, though not as high as in the USA, are increasing year upon year within both countries (Office for National Statistics, 2018 & Mervosh, 2018). This preliminary study looked into using Micro-CT scanning as a method to visualise impact damage and spray patterns caused by 12 test firings of both round and flat nosed bullets to porcine bone (shoulder and leg) suspended in ballistic gelatine and left with no covering, covered with a skin substitute, or covered with fabric (cotton or denim). Micro-CT scanning alongside VG Studio Max showed that overall, in the case of the shoulder bones the round nosed produced longer spray patterns (35.37 mm) within the gelatine blocks compared to the flat nosed bullet (27.33 mm); while with the leg bones the spray patterns were shorter, round nosed bullet (15.64 mm) and the flat nosed bullet (20.78 mm). These initial results showed that both bullet types produced considerable damage, from splitting to full penetration, which in turn illustrates how Micro-CT scanning has benefits within forensic ballistics, which should be further investigated.

Using µX-Ray CT to observe postmortem diffusion from the stomach in a rat model.

The stomach has long been recognised as a depot for postmortem diffusion. A better understanding of the phenomena of postmortem diffusion would aid forensic practitioners in their interpretation of toxicological results. A limitation of previous stomach diffusion studies was the lack of ability to visualise postmortem diffusion in real time, the use of µX-ray Computed Tomography (CT) could overcome this problem. We utilised CT to track the diffusion of the contrast medium caesium ions (Cs+) (administered by oral gavage) from the rat stomach over 6 days. We investigated the influence of temperature (4°C and 20°C) and body position (horizontal and vertical). The results show that the a) diffusion of Cs+ from the stomach can be visualised over 6 days, over which a significant amount (∼50%) of the diffusion occurs in the first 24h following administration; b) storing the rat at 4°C reduces the distance of diffusion from the stomach by ∼66%; c) body position influences the route of diffusion and d) in 2 of the 16 rats studied Cs+ was found in the right lobe of the liver. Overall these results show that CT using Cs+ is a good model to visualise postmortem diffusion and that bodies show significant variation in postmortem diffusion. It is also clear that bodies should be refrigerated and postmortem samples should be taken as soon as possible to minimise the influences of postmortem diffusion from the stomach.

The expression of affect in African elephant (Loxodonta africana) rumble vocalizations.

Affective states are thought to be expressed in the mammalian voice, but such investigations are most common in primates. Source and filter features of rumbles were analyzed from 6 adult female African elephants (Loxodonta africana) at Disney's Animal Kingdom. Rumbles produced during periods of minimal social interaction ("low affect") were compared to those produced during dominance interactions ("high affect"). Low-ranking females produced rumbles with increased and more variable fundamental frequencies, and increased durations and amplitudes during dominance interactions with superiors, compared to the low affect context. This acoustic response is consistent with the expression of affect in mammals and may signal submission to superiors. The 2 highest ranking females were codominant and competed for alpha status. They produced rumbles with decreased and less variable fundamental frequencies, increased durations and amplitudes, and a decrease in formant dispersion during dominance interactions with each other, compared to the low affect context. This response is not generally consistent with the expression of affect, but may signal large body size to competitors. These results suggest that affect can be expressed in the voiced sounds of elephants.

GPS determination of walking rates in captive African elephants (Loxodonta africana).

The movements of elephants in captivity have been an issue of concern for animal welfare activists and zoological professionals alike in recent years. In order to fully understand how movement rates reflect animal welfare, we must first determine the exact distances these animals move in the captive environment. We outfitted seven adult female African elephants (Loxodonta africana) at Disney's Animal Kingdom with collar-mounted global positioning recording systems to document their movement rates while housed in outdoor guest viewing habitats. Further, we conducted preliminary analyses to address potential factors impacting movement rates including body size, temperature, enclosure size, and social grouping complexity. We found that our elephants moved at an average rate of 0.409+/-0.007 km/hr during the 9-hr data collection periods. This rate translates to an average of 3.68 km traveled during the observation periods, at a rate comparable to that observed in the wild. Although movement rate did not have a significant relationship with an individual's body size in this herd, the movements of four females demonstrated a significant positive correlation with temperature. Further, females in our largest social group demonstrated a significant increase in movement rates when residing in larger enclosures. We also present preliminary evidence suggesting that increased social group complexity, including the presence of infants in the herd, may be associated with increased walking rates, whereas factors such as reproductive and social status may constrain movements.