Pied tamarins change their vocal behavior in response to noise levels in the largest city in the Amazon.

Many animal species depend on sound to communicate with conspecifics. However, human-generated (anthropogenic) noise may mask acoustic signals and so disrupt behavior. Animals may use various strategies to circumvent this, including shifts in the timing of vocal activity and changes to the acoustic parameters of their calls. We tested whether pied tamarins (Saguinus bicolor) adjust their vocal behavior in response to city noise. We predicted that both the probability of occurrence and the number of long calls would increase in response to anthropogenic noise and that pied tamarins would temporally shift their vocal activity to avoid noisier periods. At a finer scale, we anticipated that the temporal parameters of tamarin calls (e.g., call duration and syllable repetition rate) would increase with noise amplitude. We collected information on the acoustic environment and the emission of long calls in nine wild pied tamarin groups in Manaus, Brazil. We found that the probability of long-call occurrence increased with higher levels of anthropogenic noise, though the number of long calls did not. The number of long calls was related to the time of day and the distance from home range borders-a proxy for the distance to neighboring groups. Neither long-call occurrence nor call rate was related to noise levels at different times of day. We found that pied tamarins decreased their syllable repetition rate in response to anthropogenic noise. Long calls are important for group cohesion and intergroup communication. Thus, it is possible that the tamarins emit one long call with lower syllable repetition, which might facilitate signal reception. The occurrence and quantity of pied tamarin' long calls, as well as their acoustic proprieties, seem to be governed by anthropogenic noise, time of the day, and social mechanisms such as proximity to neighboring groups.

Low-cost thermoregulation of wild sloths revealed by heart rate and temperature loggers.

Arboreal herbivores require large digestive tracts for leaf fermentation and detoxification; however, they must also have a low body mass that allows them to reach the foliage. The three-toed sloth, Bradypus tridactylus, experiences this trade-off, as leaves comprise 97.2% of its diet. Their calorie intake is extremely low owing to the low available caloric density of leaves and slow digestive processes related to leaf fibre fermentation and secondary compound detoxification. Sloths may require a high body temperature to assist fermentation; however, thermogenesis is energy-consuming. To investigate how sloths accomplish thermoregulation using marginal energy, we attached heart rate (HR) and temperature loggers to wild B. tridactylus individuals inhabiting the Amazon rainforest and recorded their HR and body surface temperature (Tskin). Tskin changed with ambient temperature (Ta) but was higher than Ta in 99.2% of cases. Increases in Tskin and HR did not coincide, suggesting that the increases were not caused by thermogenesis. Instead, they may passively increase Tskin by selecting warmer microhabitats and sunbathing. Consequently, 90.5% of Tskin were within 27.6-36.0 °C while the Ta fluctuated between 21.5 and 42.9 °C. This low-cost thermoregulation results in a low HR. In this study, the mean HR during observation was approximately 38.4% of the expected value based on the mammalian allometric relationship between body mass and HR. Thus, these properties may contribute to the low metabolic rates of sloths, alleviating their restricted energy intake.

Is zoonotic Plasmodium vivax malaria an obstacle for disease elimination?

BACKGROUND: The groundwork for malaria elimination does not currently consider the potential of Plasmodium zoonotic cycles that involve non-human primates (NHPs) in sylvatic environments. Since vivax malaria is less responsive to control measures, finding Plasmodium vivax infected NHPs adds even more concern. METHODS: Both Free-living monkeys in forest fragments inside the urban area and captive monkeys from a local zoo had blood samples tested for Plasmodium species. RESULTS: In this study, among the Neotropical monkeys tested, three (4.4%), one captive and two free-living, were found to be naturally infected by P. vivax. CONCLUSION: This important finding indicates that it is necessary to estimate the extent to which P. vivax NHP infection contributes to the maintenance of malaria transmission to humans. Therefore, the discussion on wildlife conservation and management must be incorporated into the malaria elimination agenda.

Two new surprising species of leaf-litter toad of the Rhinella margaritifera species group (Anura: Bufonidae) from the Peruvian Amazon, LoretoPeru.

We describe two new species of Rhinella (Anura: Bufonidae) from the department of Loreto, Peru. We integrate morphological and phylogenetic analyses to provide evidence of new species. R. angeli sp. nov. is diagnosable from all congeners by its pronounced fleshy proboscis and R. unapensis sp. nov. by the small size (mean snout-vent length=37.7 4.1 mm) of adult males, snout pointed in dorsal view, nearly acute in lateral view, and small bony protrusion at the angle of jaws among other characters. The two species are allopatric, where the first species is known to be associated inhabits upland (=terra firme) forests, while the second white sand forests (=varillales) around Iquitos city. The two new species represent the 20th and 21st species of the Rhinella margaritifera species group.

Microclimate and the vertical stratification of potential bridge vectors of mosquito­borne viruses captured by nets and ovitraps in a central Amazonian forest bordering Manaus, Brazil.

In the Americas, some mosquito-borne viruses such as Zika, chikungunya, and dengue circulate among humans in urban transmission cycles, while others, including yellow fever and Mayaro, circulate among monkeys in sylvatic cycles. The intersection of humans and wildlife at forest edges creates risk for zoonotic virus exchange. We built a scaffold tower at the edge of a treefall gap in rainforest bordering Manaus, Brazil, to identify vectors that may bridge transmission between humans and monkeys. We vertically sampled diurnally active, anthropophilic mosquitoes using handheld nets at 0, 5, and 9 m and container-breeding mosquitoes in ovitraps at 0, 5, 10, and 15 m. Haemagogus janthinomys and Psorophora amazonica were present in high relative abundance in nets at each height sampled, while anthropophilic species were uncommon in ovitraps. Hg. janthinomys was more abundant at elevated heights than at ground level, while Ps. amazonica abundance was not significantly stratified across heights. The presence of each species increased with increasing 7-day rainfall lagged at 1 week, and at 1 and 4 weeks prior to collection, respectively. In addition, Hg. janthinomys was most frequently collected at 29.9 °C, irrespective of height. These data provide insight into the potential role of each species as bridge vectors.

Lack of Evidence of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Spillover in Free-Living Neotropical Non-Human Primates, Brazil.

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the agent of coronavirus disease 2019 (COVID-19), is responsible for the worst pandemic of the 21st century. Like all human coronaviruses, SARS-CoV-2 originated in a wildlife reservoir, most likely from bats. As SARS-CoV-2 has spread across the globe in humans, it has spilled over to infect a variety of non-human animal species in domestic, farm, and zoo settings. Additionally, a broad range of species, including one neotropical monkey, have proven to be susceptible to experimental infection with SARS-CoV-2. Together, these findings raise the specter of establishment of novel enzootic cycles of SARS-CoV-2. To assess the potential exposure of free-living non-human primates to SARS-CoV-2, we sampled 60 neotropical monkeys living in proximity to Manaus and São José do Rio Preto, two hotspots for COVID-19 in Brazil. Our molecular and serological tests detected no evidence of SAR-CoV-2 infection among these populations. While this result is reassuring, sustained surveillance efforts of wildlife living in close association with human populations is warranted, given the stochastic nature of spillover events and the enormous implications of SARS-CoV-2 spillover for human health.

Phylogenetic relationships of the poorly known treefrog Boana hobbsi (Cochran amp; Goin, 1970) (Anura: Hylidae), systematic implications and remarks on morphological variations and geographic distribution.

Boana hobbsi is a poorly known hylid frog currently placed within the Boana punctata group. Yet, morphological, ecological and bioacoustic traits do not support this placement, with no molecular data being available to date to test this hypothesis. Based on newly collected mitochondrial DNA sequences, morphological data review and field observations, we provide new insight into the phylogenetic relationships, morphological variations and geographic distribution of B. hobbsi. Our findings reveal that B. hobbsi is nested (with strong support) within the Boana benitezi group, recovering once more a polyphyletic Boana punctata group. Supported by this new genetic, morphological and ecological evidence, we propose a new taxonomic arrangement which includes B. hobbsi as a member of the Boana benitezi group. Furthermore, we emphasize the importance of conducting biological inventories in remote Amazonian areas, where many taxonomic and geographic knowledge gaps persist with regards to Amphibian diversity.

A new species of the Rhinella margaritifera (Laurenti 1768) species group (Anura, Bufonidae) from southern Brazilian Amazonia.

Neotropical toads from the Rhinella margaritifera species group have been considered a taxonomic puzzle for a long time. Because of the high morphological similarity and an unknown number of undescribed taxa among the species of this group, we did an extensive search for character distribution within all nominal taxa. Herein we describe Rhinella parecis sp. nov. a new species from Southern Brazilian Amazon. We provide a morphological diagnosis, morphometric comparisons with similar species, and a molecular phylogenetic hypothesis on the relationships of the new species. Rhinella parecis sp. nov. is assigned to the R. margaritifera group and differs from others species by snout-vent length ranging 40.7-53.5 mm in males (n=12) and 44.9-54.8 mm in females (n=4), snout rounded in dorsal view, acute with fleshy ridge extending to tip of snout in lateral view, canthal and pre-orbital crests absent, supra-orbital, parietal and supra-tympanic crests present and low, dorsolateral row of tubercles present, bony protrusion at the angle of jaws absent, tympanum evident, vertebral apophyses absent and toes half-webbed. The new species is the 20th species associated to the R. margaritifera group distributed in the Chapada dos Parecis, a probable center of endemism in states of Rondônia and Mato Grosso, Brazil.

The vertical stratification of potential bridge vectors of mosquito-borne viruses in a central Amazonian forest bordering Manaus, Brazil.

The emergence of Zika virus (ZIKV) in Latin America brought to the fore longstanding concerns that forests bordering urban areas may provide a gateway for arbovirus spillback from humans to wildlife. To bridge urban and sylvatic transmission cycles, mosquitoes must co-occur with both humans and potential wildlife hosts, such as monkeys, in space and time. We deployed BG-Sentinel traps at heights of 0, 5, 10, and 15 m in trees in a rainforest reserve bordering Manaus, Brazil, to characterize the vertical stratification of mosquitoes and their associations with microclimate and to identify potential bridge vectors. Haemagogus janthinomys and Sabethes chloropterus, two known flavivirus vectors, showed significant stratification, occurring most frequently above the ground. Psorophora amazonica, a poorly studied anthropophilic species of unknown vector status, showed no stratification and was the most abundant species at all heights sampled. High temperatures and low humidity are common features of forest edges and microclimate analyses revealed negative associations between minimum relative humidity, which was inversely correlated with maximum temperature, and the occurrence of Haemagogus and Sabethes mosquitoes. In this reserve, human habitations border the forest while tamarin and capuchin monkeys are also common to edge habitats, creating opportunities for the spillback of mosquito-borne viruses.

Rediscovery of Osteocephalus vilarsi (Anura: Hylidae): an overlooked but widespread Amazonian spiny-backed treefrog.

Osteocephalus vilarsi (Melin, 1941) is an Amazonian treefrog species known for over 75 years from its holotype only. Due to a lack of published data on its morphological diagnostic characters and their variations, as well as the absence of molecular, acoustic and ecological data supporting its identity, a highly dynamic taxonomic history has led this species to be confused and even synonymised with other Osteocephalus species from distinct species groups. The molecular phylogenetic relationships of O. vilarsi were investigated based on recently collected specimens from eight Northwestern Brazilian localities in the state of Amazonas, leading to its removal from the Osteocephalus taurinus species group and placement in the Osteocephalus planiceps species group. Furthermore, detailed data on morphology and colour variation are provided, as well as advertisement call and tadpole descriptions. Finally, the currently known geographic range of O. vilarsi is considerably extended, first data on the natural history of the species are provided, and the possible ecological preference of O. vilarsi for Amazonian white-sand forests is discussed.

Anuran diversity in urban and rural zones of the Itacoatiara municipality, central Amazonia, Brazil / Diversidade de anuros nas zonas urbana e rural de Itacoatiara, Amazônia central, Brasil

Few studies in the Amazon region have evaluated anuran diversity in urban forest fragments or in areas with differing degrees of anthropogenic impact. We determined the composition and abundance of the anurofauna in urban and rural sites within the municipality of Itacoatiara in central Amazonia, Brazil. Specimens were sampled from January 2012 to May 2013 in 10 urban sites and five rural sites. A total of 1,538 anurans (930 in rural sites and 608 in urban sites) were recorded, belonging to 29 species in five families. Species richness was higher in rural sites, with 10 exclusive species. All species found in urban sites were also found in rural sites, however, species abundance varied considerably between the habitats. Sampling- and individual-based rarefaction curves showed a tendency toward stabilization of species richness only in the urban sites. We concluded that the anuran assemblages in the urban sites are depauperate due to the absence of many species associated to pristine terra firme or várzea and igapó forests. Habitat loss and quality degradation in urban landscapes are the main factors threatening amphibian diversity. The anuran assemblages in our study areas were similar to those recorded in other Amazonian habitats. Conservation measures involving anurans in this region should consider the preservation of habitat mosaics, including both pristine terra firme, várzea and igapó forests. (AU)

Poucos estudos avaliaram a diversidade de anuros em fragmentos florestais urbanos ou em áreas com diferentes graus de impacto antrópico na Amazônia. Neste estudo foi determinada a composição e abundância de anuros em áreas urbanas e rurais no município de Itacoatiara, na Amazônia central, Brasil. Anuros foram amostrados entre janeiro de 2012 e maio de 2013 em 10 locais na área urbana e cinco na área rural. Um total de 1.538 indivíduos (930 na área rural e 608 na área urbana) foram registrados, compreendendo 29 espécies e cinco famílias. A área rural apresentou maior riqueza de espécies, com 10 espécies exclusivas. Todas as espécies identificadas na área urbana também foram encontradas na área rural, mas a abundância das espécies entre ambas áreas variou consideravelmente. Curvas de rarefação por amostragem e por número de indivíduos tenderam à estabilização na riqueza de espécies somente na área urbana. Concluímos que a comunidade de anuros na área urbana está empobrecida devido à ausência de muitas espécies associadas à ambientes inalterados de florestas de terra firme, várzea e igapó. A degradação da qualidade e a perda de habitat nas paisagens urbanas são os principais fatores que ameaçam a diversidade de anfíbios. A comunidade de anuros registrada neste estudo foi similar às de outros habitats na Amazônia. Medidas de conservação envolvendo anuros nesta região devem considerar a preservação de um mosaico de habitats que inclua áreas naturais de floresta de terra firme, várzea e igapó.(AU)

Redescription of the Amazonian tiny tree toad Amazophrynella minuta (Melin, 1941) (Anura: Bufonidae) from its type locality.

The description of Amazophrynella minuta was published in 1941 by the Swedish naturalist Douglas Melin based on material from Taracuá (Amazonas state, Brazil). This description was very brief and based on the morphology of few specimens with diagnostic characters and color variation not well defined. Moreover, the type series is currently in poor state of conservation. Consequently, taxonomic ambiguity surrounds the nominal taxon A. minuta, which hampers the description of many unnamed congeneric species. Herein, we redescribe A. minuta based on recently collected specimens from the type locality, designate a lectotype, formulate a new diagnosis, provide patterns of morphological variation, measurements and body proportions.

On Rhinella gildae Vaz-Silva, Maciel, Bastos Pombal 2015 (Anura: Bufonidae): Phylogenetic relationship, morphological variation, advertisement and release calls and geographic distribution.

Anurans in the Rhinella margaritifera group have a long history of taxonomic confusion, mainly by morphological similarity between species and lack of acoustic and genetic data for many of the 19 described species. Herein, we presented data for Rhinella gildae based on recently collected specimens from its type locality. We provide patterns of morphological variation, measurements, advertisement and release calls and infer the phylogenetic position of R. gildae. The species geographical distribution was updated, occurring in two Amazonian localities in Maranhão state, and Cerrado areas in Maranhão and Tocantins states and also in a rainforest enclave inside Caatinga domain in Ceará state.

Description of the advertisement calls of four species of Amazophrynella (Anura:Bufonidae).

Amazophrynella comprises 11 small bufonid species with a pan-Amazonian distribution (Fouquet et al. 2012a, b; Rojas et al. 2016, Rojas et al. 2018). All species inhabit the forest leaf litter, breed in seasonal puddles and are diurnally and nocturnally active (Fouquet et al. 2012b; Rojas et al. 2014; 2015; 2016). Until now only one nominal species, A. javierbustamantei, and two putative lineages-A. moisesii (Rio Yuyapichis, Peru) and A. siona (Santa Cecilia, Ecuador)-had their advertisement calls formally described (Duellman 1978; Schlüter 1981; Rojas et al. 2016). Herein, we described for the first time the advertisement calls from additional four species of Amazophrynella.

A Pan-Amazonian species delimitation: high species diversity within the genus Amazophrynella (Anura: Bufonidae).

Amphibians are probably the most vulnerable group to climate change and climate-change associate diseases. This ongoing biodiversity crisis makes it thus imperative to improve the taxonomy of anurans in biodiverse but understudied areas such as Amazonia. In this study, we applied robust integrative taxonomic methods combining genetic (mitochondrial 16S, 12S and COI genes), morphological and environmental data to delimit species of the genus Amazophrynella (Anura: Bufonidae) sampled from throughout their pan-Amazonian distribution. Our study confirms the hypothesis that the species diversity of the genus is grossly underestimated. Our analyses suggest the existence of eighteen linages of which seven are nominal species, three Deep Conspecific Lineages, one Unconfirmed Candidate Species, three Uncategorized Lineages, and four Confirmed Candidate Species and described herein. We also propose a phylogenetic hypothesis for the genus and discuss its implications for historical biogeography of this Amazonian group.

Differential chromosomal organization between Saguinus midas and Saguinus bicolor with accumulation of differences the repetitive sequence DNA.

Saguinus is the largest and most complex genus of the subfamily Callitrichinae, with 23 species distributed from the south of Central America to the north of South America with Saguinus midas having the largest geographical distribution while Saguinus bicolor has a very restricted one, affected by the population expansion in the state of Amazonas. Considering the phylogenetic proximity of the two species along with evidence on the existence of hybrids between them, as well as cytogenetic studies on Saguinus describing a conserved karyotypic macrostructure, we carried out a physical mapping of DNA repeated sequences in the mitotic chromosome of both species, since these sequences are less susceptible to evolutionary pressure and possibly perform an important function in speciation. Both species presented 2n = 46 chromosomes; in S. midas, chromosome Y is the smallest. Multiple ribosomal sites occur in both species, but chromosome pairs three and four may be regarded as markers that differ the species when subjected to G banding and distribution of retroelement LINE 1, suggesting that it may be cytogenetic marker in which it can contribute to identification of first generation hybrids in contact zone. Saguinus bicolor also presented differences in the LINE 1 distribution pattern for sexual chromosome X in individuals from different urban fragments, probably due to geographical isolation. In this context, cytogenetic analyses reveal a differential genomic organization pattern between species S. midas and S. bicolor, in addition to indicating that individuals from different urban fragments have been accumulating differences because of the isolation between them.

Integrative overview of the herpetofauna from Serra da Mocidade, a granitic mountain range in northern Brazil.

The Brazilian mountain ranges from the Guiana Shield highlands are largely unexplored, with an understudied herpetofauna. Here the amphibian and reptile species diversity of the remote Serra da Mocidade mountain range, located in extreme northern Brazil, is reported upon, and biogeographical affinities and taxonomic highlights are discussed. A 22-days expedition to this mountain range was undertaken during which specimens were sampled at four distinct altitudinal levels (600, 960, 1,060 and 1,365 m above sea level) using six complementary methods. Specimens were identified through an integrated approach that considered morphological, bioacoustical, and molecular analyses. Fifty-one species (23 amphibians and 28 reptiles) were found, a comparable richness to other mountain ranges in the region. The recorded assemblage showed a mixed compositional influence from assemblages typical of other mountain ranges and lowland forest habitats in the region. Most of the taxa occupying the Serra da Mocidade mountain range are typical of the Guiana Shield or widely distributed in the Amazon. Extensions of known distribution ranges and candidate undescribed taxa are also recorded. This is the first herpetofaunal expedition that accessed the higher altitudinal levels of this mountain range, contributing to the basic knowledge of these groups in remote areas.

Concerted evolution in the mitochondrial control region of the Amazon small-bodied frog Pseudopaludicola canga (Anura, Leiuperidae).

This study presents evidence of concerted evolution in the mitochondrial control region of the frog Pseudopaludicola canga. Four repeat units of 88 bp (as well as a fifth, incomplete unit) were observed in the 5' domain, with the duplicated segments of the same specimen being more related to one another than to the equivalent regions in other specimens, as a result of concerted evolution. We highlight that drawing conclusions from phylogeographical analysis using the control region containing VNTRs must be interpreted with caution, because it violated a basic assumption of phylogeny, since the regions cannot be treated as independent characters.

Uncovering the diversity in the Amazophrynella minuta complex: integrative taxonomy reveals a new species of Amazophrynella (Anura, Bufonidae) from southern Peru.

A new species of the genus Amazophrynella (Anura, Bufonidae) is described from the departments of Madre de Dios, Cusco and Junin in Peru. An integrative taxonomy approach is used. A morphological diagnosis, morphometrics comparisons, description of the advertisement call, and the phylogenetic relationships of the new species are provided. Amazophrynella javierbustamantei sp. n. differs from other species of Amazophrynella by: intermediate body-size (snout-vent length 14.9 mm in males, n = 26 and 19.6 mm in females, n = 20), tuberculate skin texture of body, greatest hand length of the Amazophrynella spp. (3.6 mm in males, n = 26 and 4.6 mm in females, n = 20), venter coloration yellowish, tiny rounded black points covering the venter, and thirteen molecular autapomorphies in the 16S RNA gene. Its distribution varies from 215 to 708 m a.s.l. This discovery highlights the importance of the remnant forest in preserving the biodiversity in Peru, and increase in seven the species formally described in the genus Amazophrynella.

ResumenDescribimos una nueva especie del género Amazophrynella (Anura, Bufonidae) del Perú de los Departamentos de Madre de Dios, Cusco y Junin de Peru. Utilizamos un método de taxonomía integrativa. Obtuvimos la diagnosis morfológica, comparaciones morfométricas, descripción del canto de reproducción y las relaciones filogenéticas de la nueva especie. Amazophrynella javierbustamanteisp. n. difiere de las otras Amazophrynella spp. por poseer tamaño medio (Hocico-cloaca en machos 16.9 mm, n = 26 y en hembras 19.6 mm, n = 20); textura de la piel tuberculada; tamaños de las manos mayores (3.6 mm en machos, n = 26 y 4.6 mm en hembras, n = 20); coloración ventral amarillento-pálida, pequeños puntos redondos de color negro en el vientre y por trece autopomorfias moleculares en el gen 16S RNA. Su distribución varía desde 215 m hasta 708 m a.s.n.m. Este descubrimiento resalta la importancia de los remanentes de la selva Peruana en términos de conservación, e incrementa en siete las especies formalmente descritas en del género Amazophrynella.

ResumoDescrevemos uma nova espécie do gênero Amazophrynella (Anura, Bufonidae) dos departamentos de Madre de Dios, Cusco e Junin do Peru. Utilizamos um método de taxonomia integrativa. Apresentamos a diagnose morfológica, comparações morfométricas, descrevemos o canto de anúncio e geramos uma hipótese filogenética da nova espécie. Amazophrynella javierbustamanteisp. n. difere das outras Amazophrynella spp. por possuir tamanho médio (Comprimento rostro-cloacal 16.9 mm em machos, n = 26 e 19.6 mm em fêmeas, n=20); textura da pele tuberculada; tamanhos das mãos maiores (3.6 mm em machos, n = 26 e 4.6 mm em fêmeas, n = 20); coloração ventral amarelo-clara, coberta por pequenos pontos redondos pretos e por treze autapomorfias moleculares no gene 16S RNA. Sua distribuição varia entre os 215 m até os 708 m a.n.m. Nossa descoberta aumenta a importância dos remanescentes da floresta Peruana em termos de conservação e incrementa em sete as espécies formalmente descritas no gênero Amazophrynella.

Effects of Forest Fragmentation on Genetic Diversity of the Critically Endangered Primate, the Pied Tamarin (Saguinus bicolor): Implications for Conservation.

We analyzed DNA at 9 microsatellite loci from hair samples of 73 pied tamarins (Saguinus bicolor) located in 3 urban forest fragments and a biological reserve in the city of Manaus, Amazonas, Brazil. The forest fragments had become isolated from the continuous forest 6-15 years prior to the time of sampling. Tests for reduction in population size showed that all groups from the urban forest fragments had undergone genetic bottlenecks. Pied tamarins in this region historically formed one biological population, and the fragments were connected by high levels of gene flow. These results indicate the need to implement a conservation plan that allows for connectivity between the urban fragments, as well as protection from further constriction. Such connectivity could be achieved via the creation and protection of corridors. In addition to the current population trends explained by anthropogenic actions, the species also shows a trend of long-term demographic decline that has resulted in approximately an order of magnitude decrease and began 13 thousand years ago.