Conservation 2019 (33): 1-11

First Inventory of in the Montane Forests of the Pasco and Ucayali Regions, Peruvian Amazon

Rolando Aquino1, Luís López2,3, Rodrigo Falcón4, Silvia Dìaz1 and Hugo Gálvez5

1Facultad de Ciencias Biológicas, Universidad Nacional Mayor de San Marcos, Lima, Perú 2Universidad Nacional de la Amazonía Peruana, Iquitos, Perú 3Asociación para la Conservación de Primates Amenazados, Iquitos, Perú 4Servicio Nacional de Áreas Naturales Protegidas por el Estado, Iquitos, Perú 5Facultad de Medicina Veterinaria, Universidad Nacional Mayor de San Marcos, Lima, Perú

Abstract: There is no information on the primate communities of the montane forests of the Peruvian Amazon except in the northeast. The regions of Pasco and Ucayali have never been explored for the primates that occur there, which motivated us to conduct this study, to assess the of the primates and especially to determine the limits of the distribution of the Peruvian yellow-tailed woolly monkey (Lagothrix flavicauda). Linear transect censuses were conducted from July to October 2018 in six survey sites. In 709 km traveled, we saw 28 groups of five species. The Peruvian woolly monkey Lagothrix( lagoth- richa tschudii) and the Marañón white-fronted capuchin (Cebus yuracus) were the most sighted, with eight and seven groups, respectively. Lagothrix flavicauda was not recorded in any of the survey sites, but we do not rule out its presence in other areas, particularly in Pasco. Red howler monkey (Alouatta seniculus) groups averaged 3.4 members, ranging from 2 to 6. The black spider monkey (Ateles chamek) and C. yuracus were seen in larger groups. The largest of three groups of the Andean saddle-back tamarin (Leontocebus leucogenys), seen in two localities, was seven. Relative abundance was higher for the species sighted in Ucayali, the highest being A. chamek with 1.5 groups/10 km. In Huánuco, the geographic distribution of L. flavicauda ranges as far as the montane forest of the province of Pachitea to the southeast, between 1,900 and 2,800 m above sea level. The geo- graphic distribution of L. l. tschudii on the other hand extends to the western side of the Ucayali, to the ríos Pachitea and Pichis, and includes the montane forests of Pasco, Ucayali and part of Huánuco. Deforestation and hunting are the main threats to the survival of primates and other wildlife, particularly in Pasco and Huánuco.

Key words: Montane forest, primates, diversity, abundance, threats.

Introduction Luna 1980, 1982, 1984; Butchart et al. 1995; Cornejo 2007; Of the 47 species of primates recognized for Peru DeLuycker 2007; Shanee 2011, 2014; Shanee and Shanee (Aquino et al. 2015a), nine inhabit the montane forests of the 2011; Shanee et al. 2007a, 2008, 2013a) and, more recently, Peruvian Amazon; of them, the Peruvian yellow-tailed woolly A. miconax (Butchart et al. 1995; Cornejo et al. 2008; Shanee monkey Lagothrix flavicauda and Andean et al. 2013b, 2015). These reports provided information on Aotus miconax are endemic and are categorized on the IUCN the abundance, distribution, threats, and some behavioral and Red List as Critically Endangered (CR) and Vulnerable (VU), ecological aspects of the two species. The studies were con- respectively (IUCN 2018). Lagothrix flavicauda was listed ducted in montane forests of the northeastern Amazon, specif- among the world’s 25 most endangered species from 2006 to ically in the regions of Amazonas and San Martín, considered 2012 (Mittermeier et al. 2007, 2009, 2012). Endemism and until 2011 to encompass the range of L. flavicauda. Reports our scarce knowledge of the ecology, behavior, geographic on other Andean montane forest primates that extend into distributions, and conservation status of L. flavicauda and A. the lowland forests as well, such as the white-bellied spider miconax have motivated researchers to prioritize research on monkey (Ateles belzebuth), are largely restricted to locality these primates as indicated by the numbers of scientific reports records (Mittermeier et al. 1975; Barrio et al. 2003; Butchart in reference to L. flavicauda (Mittermeier et al. 1975; Leo et al. 1995; Shanee et al. 2007b, 2013a).

1 Aquino et al.

Figure 1. Survey sites by region for the inventory and assessments of primate abundance. The numbers correspond to the list in Table 1.

Studies on the distribution and threats to L. flavicauda forests near the villages of Santa Rosa and Juan Velazco, in have been carried out in the regions of La Libertad and Huá- the micro-basins of the ríos Previsto and Lobo. nuco by Shanee (2011), in the valley of Kcosñipata (Cusco) by Medina et al. (2012: inventory of ), in Cajamarca Methods by Aquino et al. (2014: locality records), and in San Martín and Huánuco by Aquino et al. (2015b, 2016a, 2016b, 2017: Study area inventory and conservation status). The remaining regions of The censuses were conducted in montane forests in the the central and southeastern Amazon that also have montane regions of Pasco, Huánuco and Ucayali. With the exception forests, including Pasco and Ucayali, have lacked any studies of the forests of Santa Rosa and Juan Velazco in the Ucayali of this sort. The possibility that L. flavicauda occupied mon- Region, the survey sites were intensely deforested for agricul- tane forests of the Pasco and Ucayali regions in the south- ture and cattle ranching. The remaining forest fragments suf- east of the Peruvian Amazon, near the limit with Huánuco, fered from the extraction of timber and other forest resources. was what motivated us to carry out an expedition there to Patches of primary forest were found only on very steep ter- determine the limits of the geographic distribution of L. flavi- rain. Subsistence hunting was widespread and common and cauda and identify the anthropogenic activities that constitute was most intense in the areas occupied by the descendants of threats for the survival of primates. the Ashaninka and Yanesha ethnic groups. The few primate We carried out linear transect censuses from 15 July to groups still inhabiting these forest patches were very elusive 10 August 2018 in forests near the villages of Pucayacu and and fearful in the presence of humans. Cushi, both in the micro-basin of the Río Santa Cruz, and Six survey sites were selected in three regions (Fig. 1). near the village of Tunqui in the micro-basin of the Río Huan- With the exception of Andahuaylas in Huánuco, the sites were cabamba; from 13 August to 5 September 2018 in forests chosen considering their proximity to the limit with Huánuco, near the village of Andahuaylas in the micro-basin of the accessibility, the availability of mules for rent, and the pres- Río Chorroyacu; and from 8 September to 7 October 2018 in ence of primary forest or essentially primary residual forest.

2 Primates of Pasco and Ucayali, Peru

The geographic coordinates and altitude of our camps, as well degree of disturbance due to the extraction of timber and as the level of disturbance of the forests are detailed in Table other forest resources, and subsistence hunting, and the larger 1. These survey sites were as follows. game species are scarce. The censuses were conducted from 1,350 to 1,600 m above sea level. This survey site was chosen Pasco Region specifically to determine the altitudinal range ofL. flavicauda In the micro-basin of the Río Santa Cruz, the residual in this part of the Huánuco Region. forest fragments bordering the village of Pucayacu (altitude: 1,987 m above sea level; coordinates:10°7'3''S,75°39'41''W). Ucayali Region The forest fragments were considerably degraded because of In the micro-basin of the Río Previsto, the essentially pri- timber extraction and hunting. The censuses were conducted mary remaining forests near the village of Santa Rosa, 1.5 km at altitudes ranging from 1,800 m to 2,450 m above sea level. from the border with the Huánuco Region and 4 km from the In the micro-basin of the Río Santa Cruz, the residual Federico Basadre road (Pucallpa to Lima) (altitude: 1,828 m forest fragments bordering the village of Cushi, very close above sea level; coordinates: 9°11'39''S, 75°45'19''W). These to the Huánuco Region (altitude: 1,800 m above sea level; relatively extensive forests were highly disturbed by selective coordinates: 9°57'49''S, 75°41'50''W). All of the high pri- logging, and considerable subsistence hunting. The larger mary forest was deforested for agriculture and cattle ranching, game species, including primates, however, were still pres- leaving only fragments of scrubby forest, with the arboreal ent. Censuses were conducted from 1,300 to 1,850 m above vegetation not exceeding 7 m in height, except for some emer- sea level. gent palms of up to 12 m. This forest type, locally called In the micro-basin of the Río Lobo, the forests near the bosque poñoso because of the predominance of thorny plants, village of Juan Velazco, very close to the Velo de la Novia was considerably disturbed due to the extraction of forest waterfall, located 11 km from the border with Huánuco, and resources, while hunting is no longer frequent because game 5.5 km from the Federico Basadre road (altitude: 1,149 m species, including primates, are now too scarce. The censuses above sea level; coordinates: 9°7'21''S, 75°42'17''W). Unlike were conducted from 1,950 to 2,650 m above sea level. the other survey sites, here the primary type forests showed In the micro-basin of the Río Huancabamba, the remain- only moderate disturbance from timber extraction, and hunt- ing forest fragments bordering the village of Tunqui, very ing was occasional, practiced mostly by hunters from villages close to the Yanachaga Chemillén Nacional Park (alti- neighboring Juan Velazco, so that the larger game species tude: 1,836 m above sea level; coordinates: 10°16'14''S, including primates, were still present. In this survey site, 75°32'19''W). These fragments of forest were also highly belonging to the village of Juan Velazco, timber extraction disturbed due to timber extraction and frequent hunting. The and hunting were prohibited by agreement among the mem- larger game species, including the primates, were scarce and bers of the community. The censuses were conducted from elusive. The censuses were conducted from 1,800 to 2,500 m 1,000 to 1,400 m above sea level. above sea level. Hunting in this region is mostly practiced by the com- Transect censuses munities of the Ashaninka and Yanesha ethnic groups, which The censuses were conducted in fragments of primary have a preference for primates, in particular the black spider forest and essentially primary, residual forest. We opened monkey (Ateles chamek), the meat of which they say is the three to four trails per survey site, the lengths of which, tastiest. Ateles chamek disappeared many years ago because depending on the relief, varied from 2 to 3 km. Each tran- of the lack of suitable forest. sect was walked two to three times in interleaved form. The censuses were conducted in both directions (inbound and Huánuco Region outbound) from 07:00 to 16:00. Two teams, each made up In the micro-basin of the Río Chorroyacu, the residual of a researcher and a field assistant, were mobilized -simul forest fragments near to the village of Andahuaylas (alti- taneously along the transects at an average speed of 0.6 km/ tude: 1,303 m, coordinates: 9°45'32''S, 75°35'11''W). Like hour. Each time a group was sighted, we recorded the follow- the aforementioned survey sites, forests there showed a high ing data in the field notebook: contact time, species, location

3 Aquino et al.

coordinates in UTM, altitude (m above sea level), group size (when possible the complete count), perpendicular distance of the first individual observed to the transect, height (in the ver- tical stratum of the forest), activity at the time of contact and the presence of juveniles and infants. We also recorded data related to the level of disturbance of the forest and anthropic activities. In total, we walked 709 km, equivalent to 1010 census hours. Of these, 323 km corresponded to the montane forests of Ucayali, 204 km to Pasco, and 182 km to Huánuco (Table 2).

Interviews Two people were interviewed at each survey site, all of them were over 40 years of age and native and/or residents of the community for more than 20 years. One reason for the interviews was to confirm or discard the existence of L. flavicauda in the forests surrounding their communities. To facilitate identification, we showed them photographs of this species and other primates (Fig. 2). The interviewees also provided information about such as the breeding and migra- Figure 3. Adult male Lagothrix lagothricha tschudii observed in the montane tion season and preferred species for hunting. forest of Pucayacu, Pasco.

Data Analysis abundance—the number of groups sighted/10 km walked. The small number of groups sighted of each species in The relative abundance was estimated for each region and is the survey sites of each region was not enough to determine based on the total length walked in the survey sites. This the population density, so we calculated only the relative allowed us to indicate the constant reduction and disturbance of their habitat and the severity of subsistence hunting. The average group size was determined from groups with full counts. Every time we contacted a group, we tried to count all the group members. A complete count was not pos- sible on most occasions because the groups were dispersed and exceeded 15 individuals and, besides, their elusive behav- ior in our presence, typical of primates subjected to constant hunting.

Results

Species and groups sighted We obtained 28 sightings of five species, 17 of them were in the montane forest of Ucayali, and the remainder between the regions of Pasco and Huánuco (Table 3). Night monkeys (Aotus) were seen outside the censuses in Pucayacu, thus increasing the number of species recorded to six. The Peru- Figure 2. Pucayacu resident providing information about primates that live in vian woolly monkey (Lagothrix lagothricha tschudii) (Fig. the forest near their village. 3) was the species seen most with eight groups, followed

4 Primates of Pasco and Ucayali, Peru

by A. chamek with five. The Andean saddle-back tamarin the Ashaninkas and Yaneshas for their very tasty meat, con- (Leontocebus leucogenys) was seen the least with just three stant hunting. A single individual was last observed in Anda- groups. Lagothrix flavicauda and the large-headed capuchin huaylas in 2013, while in Cushi, Pucayacu and Tunqui, they (Sapajus macrocephalus) were not seen in any of the survey have not been seen for more than 25 years, which would sites, while A. chamek and L. leucogenys were restricted to the Ucayali Region. With regard to L. flavicauda, the interviewees in Pasco and Ucayali told us that apart from the "choro cenizo" (L. lagothricha tschudii), there was no other “mono choro” in the forests surrounding their communities. In Andahuaylas, the interviewees assured us that L. flavicauda, locally known as “coto negro,” does not live in the lower elevations of the mountains, and is not present, as such, in forests close to the community but is commonly found at higher elevations, mainly between Libertad and Oso Mayo; two sites that were previously surveyed, confirming their presence there. Ateles chamek was also absent from the Pasco and Huánuco survey sites. The interviewees told us that it was common some years ago, but diminished in numbers as the years passed, until it disappeared altogether. The interview- ees indicated that the main causes were the lack of adequate Figure 4. Adult couple of Alouatta seniculus in the montane forest of Juan forests for the spider monkeys and, preferred as they are by Velazco, Ucayali.

5 Aquino et al.

yuracus groups. Ten was the maximum, incomplete count in indicate that the species is locally extinct at these sites. The a group that probably exceeded 15 individuals. red howler monkey, Alouatta seniculus, (Fig. 4) was one of the rarer species in the study area. Of the five groups sighted, Relative abundance four were in forests in Ucayali, one in Pasco, and none in According to our analysis, the highest abundance of pri- Huánuco. mates was in the Ucayali Region (Table 5). Comparing spe- Another species that we expected was S. macrocephalus, cies, L. lagothricha tschudii was the most abundant in Pasco but we failed to see it at any of the survey sites. The inter- (0.2 groups/10 km) and Huánuco (0.16 groups/10 km), while viewees in Pasco and Huánuco told us that it still exists in the scarcest were A. seniculus and C. yuracus, both in Pasco, their forests, but that it is very rare, while in Juan Velazco and with only 0.05 groups/10 km. In Ucayali, A. chamek stood Santa Rosa, they assured us that this primate lives in the lower out for its greater abundance, while L. lagothricha tschudii elevations, not in montane forests. was the least abundant with only 0.03 groups/10 km. This difference may be a result of competition for habitat and food Group size and range sources. Alouatta seniculus and L. lagothricha tschudii were the only species with complete counts of more than one group. Limits of the geographic distribution of L. flavicauda in This was facilitated by them being in smaller groups than A. Huánuco chamek and C. yuracus. The average group size of A. senicu- In Huánuco, the geographical distribution of L. flavi- lus was 3.4 (range: 2 to 6 individuals) and for L. l. tschudii cauda to the southeast reaches the montane forests of the it was 4.2 (range: 3 to 6 individuals) (Table 4); results that province of Pachitea, which borders the Pasco Region to the clearly indicate that these primates are severely hunted. south and to the east the Ucayali Region. Here, its habitat Ateles chamek groups were larger, almost all in forests sur- includes montane forest at altitudes of about 1,900 m to about rounding the village of Juan Velazco, where hunting and 2,800 m above sea level—dwarf forest, arboreal vegetation deforestation were prohibited. There, the single group with a 7 m in height (occasionally reaching 12 m), called bosque complete count was composed of 21 individuals, besides four poñoso by the locals, predominates above 2,800 m. The area dependent infants. We failed to obtain any good counts of C. inhabited by this primate is approximately 358 km², and it extends from the upper course and headwaters of the Oso

6 Primates of Pasco and Ucayali, Peru

Figure 5. Limit of the geographic distribution of L. flavicauda in the southeast of Huánuco.

Figure 6. Expansion of the range of L. lagothricha tschudii west of the Río Ucayali. Orange without points indicates previously known range and orange with points the expansion.

7 Aquino et al.

Mayo (right tributary of the Río Paujil) to Paujil (left tribu- tary of the Río Pozuzo), very close to the limit with the Pasco Region in the south, up to the upper course and headwaters of the Río Tulumayo in the north (Fig. 5).

Expansion of the geographic distribution of L. lagothricha tschudii The results obtained in this and previous studies allow us to conclude that the distribution of L. lagothricha tschudii extends towards the western banks of the ríos Ucayali, Pachitea and Pichis, from the ríos Aguaytía, Santa Ana (left tributary of the Río Aguaytía),Aspuzana (right tributary of the Río Huallaga) and Pisqui (left tributary of the Río Ucay- ali) in the north, to the Río Perené in the south (Fig. 6). This primate is also present in montane forests up to an altitude of about 2,400 m, in the Ucayali, Huánuco, Pasco and, in part, Junín regions, as was demonstrated by our sightings of groups Figure 8. Primary forest in Juan Velazco, Ucayali with primate populations at the survey sites at altitudes of 1,393 m to 2,357 m above relatively well conserved. sea level. Unlike Pasco and Huánuco, at the Ucayali survey sites Threats and current status of primates the forests were only moderately disturbed, which explains The results of the analysis for the survey sites in Pasco and the presence and relative abundance of A. chamek and other Huánuco indicate that A. chamek and S. macrocephalus are primates, particularly in forests surrounding the village of absent, while other primates, including A. seniculus, are very Juan Velazco (Fig. 8). This has much to do with the commit- scarce. This is due to the intense deforestation for agriculture, ment assumed by the villagers to ban hunting and deforesta- cattle ranching and logging (Fig. 7), but also to subsistence tion for a communal conservation area, something which will hunting, largely by the Ashaninka and Yanesha ethnic groups, benefit future generations. considered among the best hunters in the Peruvian Amazon. The absence of A. chamek for more than 20 years, indicates Discussion that it has been extirpated in the survey sites and probably also in the entire montane forest of Pasco. The scarcity of The number of species seen in this study is slightly lower these primates has resulted in hunting being directed towards than the seven reported by Aquino et al. (2017) for Huánuco- other mammals, including large rodents such as the pacarana San Martín. It is the same, however, as that reported by (Dinomys branickii), lowland paca (Cuniculus paca), moun- Shanee et al. (2013a) for the premontane and montane for- tain paca (Cuniculus taczanowskii), and brown agouti (Dasy- ests of Monzón and Ajenco, both in the Huánuco Region, and procta variegata). those obtained for the montane forests of Cajamarca (Aquino et al. 2014) and Chontayacu-Miraflores (Aquinoet al. 2016b), all with six species. It is greater than that provided by Barrio et al. (2003) for the area between Laguna de los Cóndores and Los Chilchos and by Medina et al. (2012) for the montane for- ests of Kcosñipata, with four and three species, respectively. Of the six recorded in this study, four were seen in Pasco and five in Ucayali, among them A. chamek not recorded during the censuses in any of the survey sites corresponding to Pasco and Huánuco, where it would seem it has been extirpated. The only A. chamek group with a complete count had 21 individuals. Two other, incompletely counted groups had at least eight and 10 individuals, which allows us to argue that the black spider monkey groups were larger than those reported for Miraflores in Huánuco, where they varied from three to 15 individuals (Aquino et al. 2015b). The groups of L. lagoth- richa tschudii, on the other hand, were smaller in size and range than those recorded in the interfluvium between the ríos Urubamba-Tambo (Aquino et al. 2013), which varied from Figure 7. Mules transporting sawn timber of Cedrela odorata illegally logged 12 to 15 individuals. In the case of A. seniculus, groups were in forests near the village Andahuaylas, Huánuco. also smaller than those reported for Chontayacu-Miraflores

8 Primates of Pasco and Ucayali, Peru

(Aquino et al. 2015b), but similar to those we have seen Huánuco and San Martín. Fortunately, there are still relatively in Chilchos, where groups did not exceed six individuals large fragments of essentially primary residual forests in the (Aquino et al. 2018). We were unable to obtain complete survey sites in Ucayali. In these forests, populations of A. counts of C. yuracus, so it is difficult to compare group sizes chamek and other primates are still found in conditions simi- with results obtained elsewhere. Groups seen in Juan Velazco lar to those reported for Miraflores and other micro-basins, are probably similar, however, to those reported by Aquino et including Chontayacu and Yanajanca (Aquino et al. 2015b). al. (2018) for Chilchos, where complete counts identified 22 These forests should be seen as immensely valuable for their individuals. On one occasion in Juan Velazco we counted a potential conservation and ecotourism, especially those near group of 10 capuchins, but we believe that there were at least to the village Juan Velazco, where primates, excepting L. l. 15 individuals because of moving branches and calls. tschudii, were still relatively abundant. The relative abundance of L. lagothricha tschudii in Hunting is the other major threat to primates, particularly Pasco was higher than was estimated for Huánuco and Ucay- in Pasco and Huánuco, hunted by the indigenous communi- ali (this study), but similar to that reported for the interfluvium ties of the Ashaninka and Yanesha ethnic groups, resulting in of the ríos Urubamba-Tambo (Aquino et al. 2013). Alouatta the extirpation of their preferred spider monkeys (A. chamek) seniculus and C. yuracus were less abundant in Pasco than and the suppression of the populations of the other species. in Ucayali (this study), San Martín-Huánuco (Aquino et al. In Juan Velazco, there is still some hunting by outsiders from 2017), Cajamarca (Aquino et al. 2014) and Chontayacu-Mira- other villages, but the communities’ practice of conserving flores (Aquino et al. 2015b). These differences have a lot to their forests and prohibiting hunting means that A. chamek do with the quality and extent of the forest. While in some can be seen with some frequency, even near the village. they are still in a good state of conservation, in others they are very much disturbed, for example in the Pasco survey sites Acknowledgments and some of those in Huánuco where primates are also heav- ily hunted. Global Wildlife Conservation’s Primate Action Fund and Until proven otherwise, for now the distribution limit of Primate Conservation Inc. kindly provided funding to carry L. flavicauda towards the southeast of the Peruvian Amazon out the first evaluation of primates in the montane forests of would be the montane forests of the province of Pachitea Pasco and Ucayali. We also thank the field assistants of the in Huánuco, coinciding with the findings of Aquino et al. Pucayacu, Cushi and Tunqui villages in Pasco, Andahuaylas (2016b), who mention the montane forests of Huánuco near in Huánuco and Santa Rosa and Juan Velazco in Ucayali, who the limits with the regions of Pasco and Ucayali. In this helped us so to achieve our objectives. We are most grateful regard, although in this study we were unable to register L. to the local authorities of these villages for helping us with flavicauda in the survey sites of Pasco and Ucayali, it may the logistics. We thank Anthony B. Rylands for polishing the still there, particularly in the Pasco Region, and needed are English. further surveys to the south, even to the montane forests of the Junín Region, because we suspect that the limit of its Literature Cited range will surpass even the montane forests to the south of Pasco. On the other hand, the expansion of the distribution Aquino, R. and F. Encarnación. 1994. Primates of Peru / Los of L. lagothricha tschudii determined in this study contrasts Primates del Perú. Primate Report 40: 130pp. with the limits proposed by Aquino and Encarnación (1994), Aquino, R., F. Cornejo and E. H. Heymann. 2013. Pri- Rylands and Mittermeier (2013), and Aquino et al. (2015a), mate abundance and habitat preferences on the lower who considered that they extended only to the eastern side of Urubamba and Tambo rivers, central-eastern Peruvian the rios Pachitea and Pichis up to the Río Ucayali and south Amazonia. 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Author’s addresses: Rolando Aquino, Facultad de Ciencias Biológicas, Universi- dad Nacional Mayor de San Marcos, Lima, Perú; Luís López, Universidad Nacional de la Amazonía Peruana, Iquitos, Perú; Rodrigo Falcón, Servicio Nacional de Áreas Naturales Pro- tegidas por el Estado, Iquitos, Perú; Silvia Dìaz, Facultad de Ciencias Biológicas, Universidad Nacional Mayor de San Marcos, Lima, Perú; and Hugo Gálvez, Facultad de Medic- ina Veterinaria, Universidad Nacional Mayor de San Marcos, Lima, Perú.

Received for publication: 14 December 2018 Revised: 18 January 2019

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