Climate determines transmission hotspots of Polycystic Echinococcosis, a life-threatening zoonotic disease, across Pan-Amazonia.

Polycystic Echinococcosis (PE), a neglected life-threatening zoonotic disease caused by the cestode Echinococcus vogeli, is endemic in the Amazon. Despite being treatable, PE reaches a case fatality rate of around 29% due to late or missed diagnosis. PE is sustained in Pan-Amazonia by a complex sylvatic cycle. The hunting of its infected intermediate hosts (especially the lowland paca Cuniculus paca) enables the disease to further transmit to humans, when their viscera are improperly handled. In this study, we compiled a unique dataset of host occurrences (~86000 records) and disease infections (~400 cases) covering the entire Pan-Amazonia and employed different modeling and statistical tools to unveil the spatial distribution of PE's key animal hosts. Subsequently, we derived a set of ecological, environmental, climatic, and hunting covariates that potentially act as transmission risk factors and used them as predictors of two independent Maximum Entropy models, one for animal infections and one for human infections. Our findings indicate that temperature stability promotes the sylvatic circulation of the disease. Additionally, we show how El Niño-Southern Oscillation (ENSO) extreme events disrupt hunting patterns throughout Pan-Amazonia, ultimately affecting the probability of spillover. In a scenario where climate extremes are projected to intensify, climate change at regional level appears to be indirectly driving the spillover of E. vogeli. These results hold substantial implications for a wide range of zoonoses acquired at the wildlife-human interface for which transmission is related to the manipulation and consumption of wild meat, underscoring the pressing need for enhanced awareness and intervention strategies.

Large-scale population disappearances and cycling in the white-lipped peccary, a tropical forest mammal.

Many vertebrate species undergo population fluctuations that may be random or regularly cyclic in nature. Vertebrate population cycles in northern latitudes are driven by both endogenous and exogenous factors. Suggested causes of mysterious disappearances documented for populations of the Neotropical, herd-forming, white-lipped peccary (Tayassu pecari, henceforth "WLP") include large-scale movements, overhunting, extreme floods, or disease outbreaks. By analyzing 43 disappearance events across the Neotropics and 88 years of commercial and subsistence harvest data for the Amazon, we show that WLP disappearances are widespread and occur regularly and at large spatiotemporal scales throughout the species' range. We present evidence that the disappearances represent 7-12-year troughs in 20-30-year WLP population cycles occurring synchronously at regional and perhaps continent-wide spatial scales as large as 10,000-5 million km2. This may represent the first documented case of natural population cyclicity in a Neotropical mammal. Because WLP populations often increase dramatically prior to a disappearance, we posit that their population cycles result from over-compensatory, density-dependent mortality. Our data also suggest that the increase phase of a WLP cycle is partly dependent on recolonization from proximal, unfragmented and undisturbed forests. This highlights the importance of very large, continuous natural areas that enable source-sink population dynamics and ensure re-colonization and local population persistence in time and space.

Ultrasound evaluation of fetal bone development in the collared (Pecari tajacu) and white-lipped peccary (Tayassu pecari).

The study of fetal development allows for evaluating the different strategies adopted by mammal species to maximize neonatal survival. Autonomous locomotion is fundamental for newborns to perform foraging activities and increases newborn survival from predation. In this study, we assess the gestational bone development of 53 collared (CP, Pecari tajacu) and 61 white-lipped (WLP, Tayassu pecari) peccaries, collected through the collaboration of subsistence hunters in the Amazon. The bone mineralization and biometry of the axial and appendicular skeleton were assessed by ultrasound examinations, and the timing of the main bone developmental events was calculated in relation to the total dorsal length (TDL) and the percentage of the total gestational period (GP). The first US signs of mineralization of the axial skeleton in CP and WLP were observed in fetuses with 3.4 cm (42 gestation days, 30% GPCP ) and 5.1 cm (51 gestation days, 32% GPWLP ). The early development of the appendicular skeleton was observed by the synchronic appearance of the mineralized scapula, humerus, radius, ulna, ilium, ischium, femur, tibia, and fibula at 36% GPCP (50 gestation days), and 35% GPWLP (56 gestation days). The pubis was mineralized in fetuses at 55% GPCP (75 gestation days) and 59% GPWLP (94 gestation days). The mineralization was observed in all autopod bones at 79% GPCP (109 gestation days) and 67% GPWLP (106 gestation days). All primary ossification centers in long bones of thoracic and pelvic limbs were mineralized in advanced fetuses (GPCP and GPWLP ≥75%). The mineralized patella was not observed in advanced fetuses in either species. Secondary ossification centers first appeared at the distal epiphysis of the femur in the CP (99 gestation days, 72% GPCP ) and the distal epiphysis of the radius, femur, and tibia in the WLP (106 gestation days, 67% GPWLP ). Advanced fetuses of CP and WLP presented 60% (15/25) and 68% (17/25) of the total secondary ossification centers observed present in the adult domestic pig, while newborns from the domestic pig presented 52% (13/25). The early intrauterine development of the skeletal system in both peccary species suggests a precocial development strategy, which likely correlates with neonatal ability to escape predators and reduces the dependence on parental care.

Wild meat trade over the last 45 years in the Peruvian Amazon.

The trade in wild meat is an important economic component of rural people's livelihoods, but it has been perceived to be among the main causes of the decline of wildlife species. Recently, the COVID-19 pandemic has brought to light an additional concern of wildlife markets as a major human-health challenge. We analyzed data from the largest longitudinal monitoring (1973-2018) of the most important urban wild-meat markets in Iquitos, Peru, to examine the trends in and impacts of these markets on people's livelihoods. Over the last 45 years, wild meat sales increased at a rate of 6.4 t/year (SD 2.17), paralleling urban population growth. Wild meat sales were highest in 2018 (442 t), contributing US$2.6 million (0.76%) to the regional gross domestic product. Five species of ungulates and rodents accounted for 88.5% of the amount of biomass traded. Vulnerable and Endangered species represented 7.0% and 0.4% of individuals sold, respectively. Despite growth in sales, the contribution of wild meat to overall urban diet was constant: 1-2%/year of total meat consumed. This result was due to greater availability and higher consumption of cheaper meats (e.g., in 2018, poultry was 45.8% cheaper and was the most consumed meat) coupled with the lack of economic incentives to harvest wild meat species in rural areas. Most wild meat was sold salted or smoked, reducing the likelihood of foodborne diseases. Community-based wildlife management plans and the continued trade bans on primates and threatened taxa may avoid biodiversity loss. Considering the recent COVID-19 pandemic, future management plans should include potential viral hosts and regulation and enforcement of hygiene practices in wild-meat markets.

Comercio de Carne de Monte en los Últimos 45 Años en la Amazonia Peruana Resumen El comercio de carne de monte es un componente económico importante del sustento de habitantes de zonas rurales, pero se ha percibido como una de las principales causas de la declinación de especies de vida silvestre. Recientemente, la pandemia de COVID-19 ha traído a la luz una preocupación adicional de los mercados de vida silvestre como un reto importante para la salud humana. Analizamos datos del monitoreo longitudinal más extenso (1973-2018) de los mercados urbanos de carne de monte más importantes en Iquitos, Perú, para examinar las tendencias y los impactos de estos mercados sobre el sustento de los habitantes. Las ventas de carne de monte incrementaron en los últimos 45 años a una tasa de 6.4 t/año (DS 2.17), en paralelo con el crecimiento de la población. Las ventas de carne de monte fueron más altas en 2018 (442 t), aportando U.S. $2.6 millones (0.76%) al producto interno bruto de la región. Cinco especies de ungulados y roedores comprendieron el 88.5% de la biomasa comercializada. Especies vulnerables y en peligro representaron 7.0% y 0.4% de los individuos vendidos, respectivamente. A pesar del incremento de las ventas, la contribución de la carne de monte al total de la dieta urbana fue constante: 1-2%/año del total de carne consumida. Este resultado se debió a una mayor disponibilidad y consumo de carnes más baratas (e. g., en 2018 la carne de pollo fue 45.8% más barata y fue la más consumida) aparejado con la falta de incentivos económicos para cosechar carne de especies silvestres en áreas rurales. La mayor parte de la carne de monte se vendía salada o ahumada, reduciendo con ello la probabilidad de enfermedades transmitidas por alimentos. Los planes de manejo de vida silvestre basados en comunidades y la prohibición continua del comercio de primates y taxa amenazados pueden evitar la pérdida de biodiversidad. Considerando la reciente pandemia de COVID-19, los planes de manejo futuros deben incluir potenciales huéspedes virales y la regulación y aplicación de prácticas de higiene en los mercados de carne de especies silvestres.

Age at sexual maturity, first parturition and reproductive senescence in wild lowland pacas (Cuniculus paca): Implications for harvest sustainability.

Generation length (GL) of a mammal, calculated through the age at sexual maturity, first reproduction and reproductive senescence can be used to assess the capacity of a population of a species to withstand differing amounts of hunting pressure by humans without depletion of animal numbers. Due to the lack of reproductive data for wild mammals, the GL is often difficult to determine for most species. In the present study, the GL parameters were assessed for the wild lowland paca (Cuniculus paca) from a sample of 119 female genitalia obtained during a 15-year hunter participatory program in the Amazon. The probability of female pacas being sexually active, with observable ovarian functionality or pregnancy, increased as both body and genitalia masses increased. The average body mass at puberty was 5.46 kg. Puberty was estimated to occur at 4 months of age, from which there was estimation when age at first parturition would occur 9 months after birth. Additionally, there was no indication that there was a decrease in parturition rate at more advanced ages. The estimated age of first reproduction for pacas was much less than previous estimates, most from assessments of captive animals. In addition, because there was no evidence of reproductive senescence, it is suggested that the average age of mature hunted pacas should be used to determine optimal harvesting rates of pacas by humans. The present study highlights the importance of in situ studies on reproduction of animals in their natural habitat because these will yield more accurate reproductive variable estimates than those obtained from captive animals. It is suggested that similar methods be used to accurately assess reproductive parameters of other tropical species that are hunted by humans.

Embryonic and fetal development of the red brocket deer (Mazama americana).

The red brocket deer (Mazama americana), a medium-sized Neotropical ungulate, is one of the most hunted mammals in the Amazon. This study analyzes the intrauterine development in the red brocket deer through the description of the external and internal morphology in one embryo and 38 fetuses collected from animals hunted for subsistence in the Amazon. The chronological order of occurrence of external characteristics in relation to the total dorsal length (TDL) was: differentiated genitalia, limbs and eyelid buds (TDL = 3.9 cm), fusioned eyelids, outer ear and hooves (TDL ≥ 9.5 cm), skin (TDL ≥ 20.4 cm), tactile pelage and nasal pigmentation (TDL ≥ 21.5 cm), covering pelage and skin spots (TDL ≥ 31.3 cm), and teeth eruption and opened eyelids (TDL ≥ 34.2 cm). The formula of fetal age was ∛W = 0.072 (t - 42), with a high linear relationship between TDL and gestational age. Multiple linear and non-linear regressions showed strong positive associations between biometric measures and absolute visceral weights with TDL. The relative weight of the tubular gastrointestinal organs, spleen and thymus increased during the fetal development; in contrast, the liver and kidneys' relative weight diminished during the fetal development. Advanced fetuses (≥44.0 cm TDL) had lower proportion of liver and larger tubular gastrointestinal organs within the visceral weight than adults. The chronology of appearance of the main events of the fetal development suggests that the red brocket deer adopt some precocial features, such as the early development of the sensorial function, including the early development of eyelids, outer ear and tactile pelage, the early development of the covering pelage which acts in thermoregulation and the early teeth eruption which allows the early foraging. Nevertheless, the precocial level of the red brocket deer is apparently lower than other species more frequently predated by large felids, such as peccaries and the paca.

Embryonic and fetal development of the white-lipped peccary (Tayassu pecari).

The white-lipped peccary (Tayassu pecari) is an endangered large-sized Neotropical ungulate that is one of the most hunted mammals in the Amazon. Here, we used two embryos and 102 white-lipped peccary fetuses originated from animals hunted for subsistence in the Peruvian and Brazilian Amazon to describe the intrauterine development of external and internal morphology of this Neotropical ungulate. Logistic regressions were used to estimate the probability of occurrence of main external characteristics in relation to the total dorsal length (TDL), while multiple linear and non-linear regressions were conducted to assess the relationship between external and visceral biometry with TDL. External characteristics appeared in the following chronological order: limbs, differentiated genitalia and opened eyelids (≥5.1 cm TDL), fused eyelids (≥6.2 cm TDL), hooves and outer ear (≥7.9 cm TDL), dorsal gland (≥9.4 cm TDL), skin (≥11.5 cm TDL); tactile pelage (≥13.8 cm TDL), covering pelage (≥20.9 cm TDL), tooth eruption (≥26.4 cm TDL) and opened eyelids (≥27.8 cm TDL). The formula of fetal age was ∛W = 0.084 (t - 31.80), with a high linear relationship between TDL and gestational age. All external biometric parameters and absolute volume of visceral organs showed strong positive relationship with TDL. Except for the liver, we found differences in the relative volume of most visceral organs between advanced fetuses (≥34.2 cm TDL) and adults. The most important events during the intrauterine development in the white-lipped peccary show that, in contrast with the domestic pig, it is a highly precocial species producing newborns with a high fetal growth velocity which allows newborns to achieve an early autonomous functionality. Our results are relevant to improve imaging techniques and assist the reproductive and clinical management for the white-lipped peccary both in captivity and in the wild.

Major shifts in Amazon wildlife populations from recent intensification of floods and drought.

In the western Amazon Basin, recent intensification of river-level cycles has increased flooding during the wet seasons and decreased precipitation during the dry season. Greater than normal floods occurred in 2009 and in all years from 2011 to 2015 during high-water seasons, and a drought occurred during the 2010 low-water season. During these years, we surveyed populations of terrestrial, arboreal, and aquatic wildlife in a seasonally flooded Amazonian forest in the Loreto region of Peru (99,780 km2 ) to study the effects of intensification of natural climatic fluctuations on wildlife populations and in turn effects on resource use by local people. Shifts in fish and terrestrial mammal populations occurred during consecutive years of high floods and the drought of 2010. As floods intensified, terrestrial mammal populations decreased by 95%. Fish, waterfowl, and otter (Pteronura brasiliensis) abundances increased during years of intensive floods, whereas river dolphin and caiman populations had stable abundances. Arboreal species, including, macaws, game birds, primates, felids, and other arboreal mammals had stable populations and were not affected directly by high floods. The drought of 2010 had the opposite effect: fish, waterfowl, and dolphin populations decreased, and populations of terrestrial and arboreal species remained stable. Ungulates and large rodents are important sources of food and income for local people, and large declines in these animals has shifted resource use of people living in the flooded forests away from hunting to a greater reliance on fish.

Assessment of mammal reproduction for hunting sustainability through community-based sampling of species in the wild.

Wildlife subsistence hunting is a major source of protein for tropical rural populations and a prominent conservation issue. The intrinsic rate of natural increase. (rmax ) of populations is a key reproductive parameter in the most used assessments of hunting sustainability. However, researchers face severe difficulties in obtaining reproductive data in the wild, so these assessments often rely on classic reproductive rates calculated mostly from studies of captive animals conducted 30 years ago. The result is a flaw in almost 50% of studies, which hampers management decision making. We conducted a 15-year study in the Amazon in which we used reproductive data from the genitalia of 950 hunted female mammals. Genitalia were collected by local hunters. We examined tissue from these samples to estimate birthrates for wild populations of the 10 most hunted mammals. We compared our estimates with classic measures and considered the utility of the use of rmax in sustainability assessments. For woolly monkey (Lagothrix poeppigii) and tapir (Tapirus terrestris), wild birthrates were similar to those from captive populations, whereas birthrates for other ungulates and lowland-paca (Cuniculus paca) were significantly lower than previous estimates. Conversely, for capuchin monkeys (Sapajus macrocephalus), agoutis (Dasyprocta sp.), and coatis (Nasua nasua), our calculated reproductive rates greatly exceeded often-used values. Researchers could keep applying classic measures compatible with our estimates, but for other species previous estimates of rmax may not be appropriate. We suggest that data from local studies be used to set hunting quotas. Our maximum rates of population growth in the wild correlated with body weight, which suggests that our method is consistent and reliable. Integration of this method into community-based wildlife management and the training of local hunters to record pregnancies in hunted animals could efficiently generate useful information of life histories of wild species and thus improve management of natural resources.

Social behavior in fission-fusion groups of red uakari monkeys (Cacajao calvus ucayalii).

Primates living in large groups that divide to forage must have social systems compatible with this mode of living. Uakari monkeys (Cacajao spp.) live in large groups and exhibit a form of fission-fusion grouping, but their social organization is poorly understood. We present some of the first data on social behavior for this genus based on a study on Cacajao calvus ucayalii. They traveled in multimale multifemale groups of highly variable sizes, with bachelor units on the periphery. Adult males were affiliative, and adult females associated with more than one adult male. Adult females typically traveled with their dependent offspring and an older juvenile within the group. In parties of two or more males, individuals engaged in previously unreported display behaviors and acted together to aggressively chase other males. Breeding was seasonal, and mating occurred away from other group members. We speculate on the social organization of C. calvus ucayalii, in which dispersal may be bisexual and peripheral males are affiliative with one another. Affiliated males appear to cooperate in fighting and displaying to other males for access to females during the breeding season.

Ovarian features of the wild collared peccary (Tayassu tajacu) from the northeastern Peruvian Amazon.

In this study, the ovaries of 27 wild collared peccaries (Tayassu tajacu) from the Amazonian region of northeastern Peru were examined macroscopically and microscopically, and expression of major steroidogenic enzymes was detected by immunohistochemistry. Our observations suggest a mean ovulation rate of 2.3 +/- 0.6 follicles and a low rate of reproductive wastage (0.4 +/- 0.6 oocytes or embryos per pregnancy). The collared peccary seems to exhibit follicular waves involving the synchronous growth of a cohort of follicles, several of which seem to attain selection. The presence of antral follicles in pregnant females suggests that follicular turnover continues during pregnancy. In cyclic animals, corpora lutea were characterised by the presence of distinct large and small luteal cell populations. The luteal volume in pregnant females was larger than that recorded for non-pregnant females. Through immunohistochemistry, it was observed that luteal cells from active corpora lutea exhibit intensive 3beta-HSD expression in advanced stages of pregnancy. This suggests that the corpora lutea seems to remain steroidogenically active throughout pregnancy and likely contribute to progesterone production during pregnancy.

Influence of digestive morphology on resource partitioning in Amazonian ungulates.

Resource partitioning of diet and habitat use was studied in the entire Amazonian ungulate community of Northeastern Peru, which comprises the red brocket deer (Mazama americana), grey brocket deer (M. gouazoubira), collared peccary (Tayassu tajacu), white-lipped peccary (T. pecari), and lowland tapir (Tapirus terrestris). Each ungulate species partitioned at least one type of resource from every other species. Digestive morphology had a greater influence on resource partitioning of diet than body size. Neither digestive morphology nor body size were related to segregation of habitats. However, species with similar diets partitioned habitats, whereas species with different diets often used the same type of forest. Increases in habitat breadth of ungulates were positively correlated with increases in dietary breadth.

Ungulate biomass in relation to feeding strategy within Amazonian forests.

The relationship between diet and biomass was examined in the Amazonian ungulates (red brocket deer, grey brocket deer, collared peccary, white-lipped peccary, and lowland tapir) of Northeastern Peru. Tropical forest ungulates have lower biomasses than savanna or grassland ungulates, because in tropical forests the majority of primary production occurs in the canopy, well out of reach from terrestrial herbivores. Within the Amazonian ungulates, species that supplement their diet with animal material, namely the peccaries, obtain a greater crude and metabolic biomass, and higher reproductive rates than the purely herbivorous species. Omnivory appears to help terrestrial herbivores inhabiting closed canopy forests overcome some effects of food limitation.