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Medium and large sized mammals and the effect of habitat heterogeneity from a Caatinga shrubby forest at Serra de Santa Catarina, Paraíba, Brazil

Abstract

In xeric environments, such as Caatinga Biome, habitat characteristics such as phytophysiognomy type and presence of water bodies can represent higher resource availability. In this context, the present study investigated the effect of phytophysiognomies and presence of water bodies in the abundance and community structure of medium and large mammal species (MLM) in the Serra de Santa Catarina, Paraíba, Brazil. To evaluate these variables we conduct an effort of 373 camera-trap days, between August 2012 and November 2014. We recorded 12 MLM species, distributed in six orders and 11 families. From those, Kerodon rupestris is the only one listed in the Brazilian List of Threatened Fauna. Regarding the habitat, the Mann-Whitney showed a significant higher frequency to the Shrubby habitat and the ANOSIM showed no shifts in the community structure between Arboreal and Shrubby. Concerning the presence of water bodies, both the Mann-Whitney and the ANOSIM showed significant higher frequency to the habitat with water presence. We observed that both phytophysiognomy and water bodies are important variables which affect mainly the abundance of mammalian species from semiarid environments. Nonetheless, whereas the forest remnants get smaller the existence of water bodies becomes a preponderant factor to the MLM species and its community structure.

Keywords:
Camera-trapping; Mammalian inventory; Habitat effect; Xeric environment

INTRODUCTION

The Caatinga biome is endemic of Brazil comprising 11% (844,453 km²) of its territory, mostly in Northeast region (Prado, 2003Prado, D. 2003. As caatingas da América do Sul. In: Leal, I.R.; Tabarelli, M. & Silva, J.M.C. Ecologia e Conservação da Caatinga. Recife, Editora Universitária p. 3-73.). Dry climate predominates, with irregular and accentuated rainfalls and prolonged droughts (Jacomine, 1996Jacomine, P.K.T. 1996. Solos sob Caatingas - Características e uso agrícola. In: Alvarez, V.; Fontes, L. & Fontes, M.P.F. O Solo nos grandes domínios morfoclimáticos do Brasil e o desenvolvimento sustentado. Viçosa, Sociedade Brasileira de Ciência do Solo; UFV. p. 95-111.; Ab’Saber, 2003Ab’Saber, A. 2003. Os domínios de natureza no Brasil. Potencialidades paisagísticas. São Paulo, Ateliê Editorial.). Caatinga is under considerable threat due to degradation and loss of habitat, with ca. 40% reduction of its original vegetation (Castelletti et al., 2003Castelletti, C.H.M.; Silva, J.M.C.D; Tabarelli, M. & Silva, J. 2003. Quanto ainda resta da Caatinga? Uma estimativa preliminar. In: Leal, I.R.; Tabarelli, M. & Da Silva, J.M.C. Biodiversidade da Caatinga: áreas e ações prioritárias para a conservação. Brasília, Ministério do Meio Ambiente; Universidade Federal de Pernambuco, p. 91-100.; MapBiomas, 2020Projeto de Mapeamento Anual do Uso e Cobertura da Terra no Brasil (MapBiomas). 2020. Coleção 5 da Série Anual de Mapas de Cobertura e Uso de Solo do Brasil. Available: Available: https://mapbiomas.org . Access: 06/12/2020.
https://mapbiomas.org...
), a direct consequence of urban, agricultural and livestock expansions (Leal et al., 2003Leal, I.R.; Tabarelli, M. & Da Silva J.M.C. 2003. Ecologia e conservação da Caatinga. Recife, Editora Universitária da UFPE.; Albuquerque et al., 2012Albuquerque, U.P.; Araújo, E.L.; El-Deir, A.CA.; De Lima, A.L.A.; Souto, A.; Bezerra, B.M.; Ferraz, E.M.N; Freire, E.M.X.; Sampaio, E.V.D.S.B.; Las-Casas, F.M.G; De Moura, G.J.B.; Pereira, G.A; De Melo, J.G.; Ramos, M.A.; Rodal, M.J.N.; Schiel, N.; De Lyra-Neves, R.M.; Alves, R.R.N.; De Azevedo-Júnior, S.M.; Telino-Júnior, W.R. & Severi, W. 2012. Caatinga revisited: ecology and conservation of an important seasonal dry forest. The Scientific World Journal, 2012: 1-18. https://doi.org/10.1100/2012/205182.). The biome’s vegetation is typically xerophilic (Oliveira et al., 2003Oliveira, J.A.; Gonçalves, P.R. & Bonvicino, C.R. 2003. Mamíferos da Caatinga. In: Leal, I.R.; Tabarelli, M. & Silva, J.M.C. Ecologia e Conservação da Caatinga. Recife, Editora Universitária da UFPE. p. 275-333.), mostly composed of trees and deciduous bushes, succulent and thorny species, and a great number of herbs and grasses (Pennington et al., 2006Pennington, R.T.; Richardson, J.E. & Lavin, M. 2006. Insights into the historical construction of species-rich biomes from dated plant phylogenies, neutral ecological theory and phylogenetic community structure. New Phytologit, 172(4): 605-616., 2009Pennington, R.T.; Lavin, M. & Oliveira-Filho, A. 2009. Woody plant diversity, evolution, and ecology in the tropics: perspectives from seasonally dry tropical forests. Annual Review of Ecology, Evolution and Systematics, 40: 437-457.), differing among regions (Andrade-Lima, 1981Andrade-Lima, D. 1981. The Caatinga dominium. Revista Brasileira de Botânica, 4: 149-153.). This reflects in the formation of diverse habitats and phytophysiognomies throughout the biome, influencing faunal components (Prado, 2003Prado, D. 2003. As caatingas da América do Sul. In: Leal, I.R.; Tabarelli, M. & Silva, J.M.C. Ecologia e Conservação da Caatinga. Recife, Editora Universitária p. 3-73.).

Mammal diversity, on the contrary, did not seem to keep up with the heterogeneity of biome’s vegetation, for a long time considered less rich and with low levels of endemism. Its species were counted as a subgroup of those found in the Cerrado (Mares et al., 1981Mares, M.A.; Willing, M.R.; Streilein, K.E. & Lacher, T.E. 1981. The mammals of northeastern Brazil: a preliminary assessment. Annals of Carnegie Museum, 50(4): 81-137., 1985; Fonseca et al., 1996Fonseca, G.A.B.; Hermann, G.; Leite, Y.L.R.; Mittermeier, R.A.; Rylands, A.B. & Patton, J.L. 1996. Lista anotada dos mamíferos do Brasil. Belo Horizonte, Conservation International. (Occasional Papers in Conservation Biology, 4); Oliveira et al., 2004Oliveira, J.A.; Coimbra-Filho, A.F.; Souto, A.; Bonvicino, C.R.; Scheibler, D.R.; Wolf, F. & Rocha, P.L.B. 2004. Mamíferos: áreas e ações prioritárias para a conservação da Caatinga. In: Silva, J.M.C.; Tabarelli, M.; Fonseca, M.T. & Lins, L.V. Biodiversidade da Caatinga: áreas e ações prioritárias para a conservação. Brasília, Ministério do Meio Ambiente, Universidade Federal de Pernambuco. p. 283-292.), which is changing with the increase of new studies. Nowadays, there are 183 registered species, 11 endemics (Gutiérrez & Marinho-Filho, 2017Gutiérrez, E. & Marinho-Filho, J. 2017. The mammalian faunas endemic to the Cerrado and the Caatinga. Zookeys, 644: 105-157. https://doi.org/10.3897/zookeys.644.10827.
https://doi.org/10.3897/zookeys.644.1082...
; Carmignotto & Astúa, 2018Carmignotto, A.P. & Astúa, D. 2018. Mammals of the caatinga: diversity, ecology, biogeography, and conservation. In: Silva, J.M.C.; Leal, I.R. & Tabarelli, M. Caatinga: the largest tropical dry forest region in South America. Switzerland, Springer. p. 211-254.). Among those species, the medium- and large-body mammals (MLM) comprise a heterogeneous polyphyletic group usually having small population size, requiring large home ranges, and cannot be collected in traditional traps designed for small mammals (i.e., Sherman and Tomahawk) (Feijó & Brandão, 2022Feijó, A. & Brandão, M.V. 2022. Taxonomy as the first step towards conservation: an appraisal on the taxonomy of medium- and large-sized Neotropical mammals in the 21st century. Zoologia, 39: 1-16. e22007.). Considering rock cavy Kerodon rupestris as a MLM, and a taxonomic catalog (Feijó & Langguth, 2013Feijó, A. & Langguth, A. 2013. Mamíferos de médio e grande porte do Nordeste do Brasil: distribuição e taxonomia, com descrição de novas espécies. Revista Nordestina de Biologia, 22: 3-225.) from the Brazilian Northeast mammals, there are 29 species occurring in the northern limits of the Caatinga domain (left bank of São Francisco River). Some of these species are considered to be threatened with extinction in some degree, including the endemic K. rupestris and Brazilian three-banded armadillo Tolypeutes tricinctus (Miranda et al., 2014Miranda, F.; Moraes-Barros, N.; Superina, M. & Abba, A.M. 2014. Tolypeutes tricinctus. The IUCN Red List of Threatened Species 2014: e.T21975A47443455.; MMA, 2022Ministério do Meio Ambiente (MMA). 2022. Portaria № 300, de 13 de dezembro de 2022. Reconhece a Lista Nacional de Espécies Ameaçadas de Extinção, conforme Anexo I desta presente Portaria. Diário Oficial da União, Edição 234, Seção 1, p. 75, 2022.).

The composition and abundance of mammal species are directly associated with habitat type and resource availability over space and time (Tews et al., 2004Tews, J.; Brose, U.; Grimm, V.; Tielbörger, K.; Wichmann, M.C.; Schwager, M. & Jeltsch, F. 2004. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography, 31: 79-92.; Stein et al., 2014Stein, A.; Gerstner, K. & Kreft, H. 2014. Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecology Letters, 17(7): 866-880.). Habitat type, heterogeneity, complexity, degrees of maturity, or disturbance in each area, play important roles in the maintenance and variation of mammal species along the landscape (August, 1983August, P.V. 1983. The role of habitat complexity and heterogeneity in structuring tropical mammal communities. Ecology, 64(6): 1495-1507.; Fonseca, 1989Fonseca, G.A.B. 1989. Small mammal species diversity in Brazilian tropical primary and secondary forests of different sizes. Revista Brasileira de Zoologia, 6(3): 381-421.; Williams et al., 2002Williams, S.E.; Marsh, H. & Winter, J. 2002. Spatial scale, species diversity, and habitat structure: small mammals in Australian Tropical Rain Forest. Ecology, 83(5): 1317-1329.; Haugaasen & Peres, 2005Haugaasen, T. & Peres, C.A. 2005. Mammal assemblage structure in Amazonian flooded and unflooded forests. Journal of Tropical Ecology, 21: 133-145.; Boron et al., 2019Boron, V.; Deere, N.J.; Xofis, P.; Link, A.; Quiñones-Guerrero, A.; Payan, E. & Tzanopoulos, J. 2019. Richness, diversity, and factors influencing occupancy of mammal communities across human-modified landscapes in Colombia. Biological Conservation, 232: 108-116.). In xeric environments (arids or semi-arids), phytophysiognomy type can represent higher (arboreal habitat) or lesser (shrubby habitat) resource availability (Freitas et al., 2005Freitas, R.R.; Rocha, P.L.B. & Simões-Lopes, P.C. 2005. Habitat structure and small mammals abundances in one semiarid landscape in the Brazilian Caatinga. Revista Brasileira de Zoologia, 22: 119-129.; Dias & Bocchiglieri, 2016Dias de, M.D. & Bocchiglieri, A. 2016. Riqueza e uso do habitat por mamíferos de médio e grande porte na Caatinga, nordeste do Brasil. Neotropical Biology and Conservation, 11: 38-46.). Meanwhile, the presence of water can be determinant for the occurrence of a variety of species, particularly water-dependent ones (mandatory drinkers) (Western, 1975Western, D. 1975. Water availability and its influence on the structure and dynamics of a savannah large mammal community. African Journal of Ecology, 13(3/4): 265-286.; James et al., 1999James, C.D.; Landsberg, J. & Morton, S.R. 1999. Provision of watering points in the Australian arid zone: a review of effects on biota. Journal of Arid Environment, 41: 87-121.).

Among current studies, most increase knowledge about mammal diversity in the Caatinga, while few investigate how different habitat conditions affect the composition and structure of the mammalian fauna. When studying habitat condition, the existing are related to small mammals (e.g.,Rocha et al., 2015Rocha, P.A.; Ruiz-Esparza, J.; Beltrão-Mendes, R.; Ribeiro, A.S.; Campos, B.A.T.P. & Ferrari, S.F. 2015. Nonvolant mammals in habitats of the Caatinga scrub and cloud forest enclave at Serra da Guia, state of Sergipe. Revista Brasileira de Zoociências, 16: 93-103.; Delciellos, 2016Delciellos, A.C. 2016. Mammals of four Caatinga areas in northeastern Brazil: Inventory, species biology, and community structure. Check List, 12: 1-15. https://doi.org/10.15560/12.3.1916.
https://doi.org/10.15560/12.3.1916...
), species with different ecological requirements compared to MLM. Meanwhile, habitat loss, hunting, trampling, forest fires, and other factors continue to negatively affect mammal species across the Caatinga (Leal et al., 2005Leal, I.R.; Da Silva J.M.C.; Tabarelli, M. & Lacher, T.E. 2005. Changing the course of biodiversity conservation in the Caatinga of northeastern Brazil\Cambiando el curso de la conservación de biodiversidad en la Caatinga del Noreste de Brasil. Conservation Biology, 19(7): 701-706.; Barboza et al., 2016Barboza, R.R.; Lopes, S.F.; Souto W.M.S; Fernandes-Ferreira, H. & Alves R.R.N. 2016. The role of game mammals as bushmeat in the Caatinga, Northeast Brazil. Ecology and Society, 21(2): 2. https://doi.org/10.5751/ES-08358-210202.
https://doi.org/10.5751/ES-08358-210202...
; Bonifácio et al., 2016Bonifácio, K.M.; Schiavetti, A. & Freire, E.M.X. 2016. Fauna used by rural communities surrounding the protected area of Chapada do Araripe. Brazilian Journal of Ethnobiology and Ethnomedicine, 12: 1-13. https://doi.org/10.1186/s13002-016-0115-x.
https://doi.org/10.1186/s13002-016-0115-...
). Species such as white-lipped peccary Tayassu pecari, collared peccary Dicotyles tajacu, jaguar Panthera onca, giant anteater Myrmecophaga tridactyla, and paca Cuniculus paca are already extinct in a great part of the biome, and historical documentation points to the total extinction of Priodontes maximus and Tapirus terrestris within this territory (Carmignotto et al., 2011Carmignotto, A.P.; Vivo, M. & Langguth, A. 2011. Mammals of the Cerrado and Caatinga: revealing distribution patterns of the tropical open biomes of South America. In: Patterson, B.D. & Costa, L.P. Historical biogeography of Neotropical mammals II: the patterns, Chicago. Chicago, Chicago University Press. v. 2, p. 307-341.; Feijó & Langguth, 2013Feijó, A. & Langguth, A. 2013. Mamíferos de médio e grande porte do Nordeste do Brasil: distribuição e taxonomia, com descrição de novas espécies. Revista Nordestina de Biologia, 22: 3-225.; Alves et al., 2016Alves, R.; Feijó, A.; Barboza, R.; Souto, W.; Fernandes-Ferreira, H.; Cordeiro-Estrela, P. & Langguth A. 2016. Game mammals of the Caatinga biome. Ethnobiology and Conservation, 5: 1-51. https://doi.org/10.15451/ec2016-7-5.5-1-51.
https://doi.org/10.15451/ec2016-7-5.5-1-...
).

Therefore, we present here the MLM species inventory of Serra de Santa Catarina (SSC), a shrub forest remnant in the Caatinga, western of Paraíba state. In addition, in a preliminary condition, we analyzed the dynamics of habitat use by species according to local phytophysiognomies (arboreal vs. shrubby) and the presence and absence of water bodies in the study area.

MATERIAL AND METHODS

Study site

The complex of Serra de Santa Catarina (SSC) is situated in the extreme west of Paraíba State (07°00′46″S, 38°11′12″W; 360-650 m asl), northeastern Brazil, in the micro-region among the municipalities of Sousa and Cajazeiras (East-West), with an area of approximately 112.1 km² (Sousa & Oliveira, 2010Sousa, P.V.P. & Oliveira, V.P.V. 2010. Evidências Paleoclimáticas no Sertão da Paraíba: redutos e rfúgios na Serra de Santa Catarina. Conferência Internacional: Clima, Sustentabilidade e Desenvolvimento em Regiões Semiáridas 16-20 de Agosto, Fortaleza - Ceará, Brasil.) (Fig. 1). The local landscape is composed by deciduous seasonal forest, dry forest, forested and arboreal steppe savanna (shrubby), with most of vegetation as arboreal, followed by shrubby and patches of herbaceous vegetation. The illegal logging, fire and hunting are the main anthropic threat that occurs in higher frequency in the region (BATPC, pers. obs.). The main precipitation season occurs between March and July, reaching ca. 900 mm of annual precipitation, with a mean annual temperature of 24℃.

Figure 1
Study area, the Serra de Santa Catarina, extreme West of Paraíba state, northeastern Brazil. In light gray Caatinga biome and in dark gray Atlantic Forest Biome; in green, Serra de Santa Catarina limits.

Data sampling

We carried out the sampling effort in four campaigns between August 2012 and November 2014, totaling 373 days of sampling, ranging from 65 to 114. We used camera-traps (Bushnell, model: 119436C) as the main sampling method, varying between campaigns (9, 4, 8, 2). Camera-traps were set to activate by motion, recording (photographs or videos) full time, with the aim of maximizing the recordings of individuals who remained at the sampling site, according to Giman et al. (2007Giman, B.; Stuebing, R.; Megum, N.; Mcshea, W.J. & Stewart, C.M. 2007. A camera trapping inventory for mammals in a mixed use planted forest in Sarawak. Raffles Bulletin of Zoology, 55: 209-215.). To assess the effect of different habitat types and conditions, we set up camera-traps in three habitat types (arboreal, shrubby, shrubby-arboreal; Fig. 2) and in two habitat conditions (presence and absence of water bodies; Fig. 2). We conducted active searches, in addition to complimentary records, through direct observations or indirect sampling through vestiges (i.e., feces, tracks, carcass/skull, fur, scarifications, burrow, and vocalizations) (Wilson et al., 1996Wilson, D.E.; Cole, F.R.; Nichols, J.D, Rudran, R. & Foster, M.S. 1996. Measuring and monitoring biological diversity - Standard methods for mammals. Washington, Smithsonian Institution Press.). These additional records were considered only for the composition of the species list. We registered some domestic animals such Bos taurus (catle) and Capra hircus (goats). They were not considered in our analysis.

Figure 2
Different habitats analyzed in Serra de Santa Catarina, Paraíba, Brazil. A=Arboreal; B=Shrub; C=Arboreal-shrub; D=Water spot with a capuchin monkey in the foreground.

Data analysis

The recorded data were classified in spreadsheets containing date, time, sampling location, habitat type (arboreal, shrubby, and shrubby-arboreal), habitat condition (absence/presence of water bodies), type of record (camera-trap and complimentary approach), species identification at the best taxonomic level, and its respective abundance. Records more than 60 min apart were considered as independent samples. For taxonomic classification and species identification, we follow Wilson & Reeder (2005Wilson, D.E. & Reeder, D.M. 2005. Mammal species of the world, a taxonomic and geographic reference. 3.ed. Baltimore, The Johns Hopkins University Press.), Nascimento & Feijó (2017Nascimento, F.O. & Feijó, A. 2017. Taxonomic revision of the tigrina Leopardus tigrinus (Schreber, 1775) species group (Carnivora, Felidae). Papéis Avulsos de Zoologia, 57(19): 231-264.), and Quintela et al. (2020Quintela, F.; Rosa, C.A. & Feijó, A. 2020. Updated and annotated checklist of recent mammals from Brazil. Anais da Academia Brasileira de Ciências, 92(Suppl. 2): 1-57. https://doi.org/10.1590/0001-3765202020191004.
https://doi.org/10.1590/0001-37652020201...
), Bernegossi et al. (2023Bernegossi, A.M.; Borges, C.H.S.; Sandoval, E.D.P.; Cartes, J.L.; Cernohorska, H.; Kubickova, S.; Vozdova, M.; Caparroz, R.; González, S. & Duarte, J.M.B. 2023. Resurrection of the genus Subulo Smith, 1827 for the gray brocket deer, with designation of a neotype. Journal of Mammalogy, 104(3): 619-633. https://doi.org/10.1093/jmammal/gyac068.
https://doi.org/10.1093/jmammal/gyac068...
). For the identification of vestiges, tracks, among others, we use field guides (e.g.,Navarro & Muñoz, 2000Navarro, J.F. & Muñoz, J. 2000. Manual de Huellas de algunos mamíferos terrestre de Colombia. Medellín Multimpressos.; Borges & Tomás, 2008Borges, P.A.L. & Tomás, W.M. 2008. Guia de rastro e outros vestígios de mamíferos do Pantanal. Corumbá, EMBRAPA Pantanal.; Júnior & Luz, 2008Júnior, O.C. & Luz, N.C. 2008. Pegadas: Séries Boas Práticas. Belém, EDUFPA.; Reis et al., 2009Reis, N.R.; Peracchi, A.L.; Fregoneze, M.N. & Rossaneis, B.K. 2009. Guia Ilustrado: Mamíferos da Serra de São Luiz do Purunã: Paraná, Brasil. Pelotas, USEB. (Manuais de Campo USEB, 12)).

Descriptive and statistical analyses were performed only with data obtained by (systematic) camera-trapping. We considered the days with effective records in different camera-traps throughout the campaigns as independent samples. We calculated the sampling effort (number of camera-traps * sampling days), and recording success (number of independent samples/sampling effort * 100), while for the rarefaction curve we used the Jackknife 1 index, calculated using EstimateS 9.0 (Colwell, 2013Colwell, R.K. 2013. EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. Available: https://purl.oclc.org/estimates.
https://purl.oclc.org/estimates...
) based on 1,000 runs. We did not conduct any seasonal analysis, as there was no regular rainfall during the samplings.

As we did not have regular ecological conditions, we performed ecological analyses as preliminary and exploratory approaches assessing the effects of habitat type (phytophysiognomies: Arboreal vs. Shrubby) and condition (Presence vs. Absence of water bodies). We consider data from different camera-traps in different field campaigns as independent samples. With regard to the analysis of the habitat type, we excluded data from the fourth campaign, as it mainly sampled the Shrubby-Arboreal phytophysiognomy, not included as a variable here. To test the above cited effects on recording success (median frequency), we use the non-parametric Mann-Whitney (according Shapiro-Wilk test). To test shifts in the structure of the MLM community, we used Analysis of Similarity (ANOSIM, one-way), represented by a Non-Metric Multidimensional Scaling (NMDS). In order to avoid the abundance bias of group-living species (mainly capuchin monkeys), we used the non-parametric indices Jackknife 1 (diversity) and Jaccard (similarity and NMDS). Analyses were run in BioEstat 5.3 (Ayres et al., 2007Ayres, M.; Ayres, J.R.M.; Ayres, D.l. & Santos A.S. 2007. BioEstat 5.0. Aplicações estatísticas nas áreas das ciências biológicas e médicas: sociedade civil Mamirauá, Belém. Brasília, CNPq. 290p.) and PAST 3.2 (Hammer et al., 2001Hammer, Ø.; Harper, D.A.T. & Ryan, P.D. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1): 9. Version 3.2. https://folk.uio.no/ohammer/past.
https://folk.uio.no/ohammer/past...
) at a significance level of 5%.

The present work does not present any ethical conflict, since we do not manipulate any live animal. The Instituto Chico Mendes de Biodiversidade (ICMBio) authorized this study through research permit (SISBio 34872-2).

RESULTS

The field effort resulted in 373 camera-trap.day sanpling effort with camera-trap, of which 118 had records that we considered independent sampling days, representing 31.6% of record success. This effort resulted in the record of 10 MLM species, in addition to two species through active searches (Euphractus sexcinctus and Galictis cuja), totaling 12 MLM for the Serra de Santa Catarina, distributed in six Orders and 11 Families (Table 1). The order Carnivora was the most represented - six species (50%), followed by Primates (n=2; 16.8%), while the remnants (Cingulata, Pilosa, Rodentia, and Artiodactyla) were represented by only one species (8.3% each).

Table 1
Taxonomic list of medium-large mammal species recorded to the Serra de Santa Catarina, West of Paraíba, Northeast Brazil, according to type of record, type of habit, and relative abundance, sampled between August 2012 and November 2014.

The observed richness (S=10) represents 77.1% for the estimated richness (S=12.97±1.7) by Jackknife 1 (Fig. 3), with no significant difference. This result suggests the record of new MLM species (3 to 5) with continued samplings. Considering that we recorded 12 species with combined methods, there may be at least three additional species yet to be recorded in the SSC.

Figure 3
Rarefaction curve for camera-trap sampling to medium-large mammal species of the Serra de Santa Catarina, Paraíba, northeastern Brazil, sampled between August 2012 and November 2014. Observed richness (S=10±1.76) has no significant difference to estimated richness (S=12.97±1.7) through the non-parametric Jackknife 1. Sample unit were defined as days with effective records in different camera-traps.

Regarding the preliminary assessment of habitat effects, the Mann-Whitney showed a significant difference both for the habitat type (arboreal vs. shrubby, U=432, p<0.05) with higher frequency to the shrubby phytophysiognomy (Fig. 4A), as for the water bodies (presence vs. absence, U=387, p<0.05) with higher frequency for the presence of water (Fig. 2b). The ANOSIM showed no shifts in community structure between habitat types (R=0.0745, p>0.05) (Fig. 5A), although there were significant differences between sites with the presence-absence of water (R=0.3126, p<0.05) (Fig. 5B).

Figure 4
Average of abundance of medium-large mammal species according to different phytophysiognomies (a) and presence of water bodies (b), recorded in the Serra de Santa Catarina, Northeast Brazil, between August 2012 and November 2014. The Mann-Whitney analysis showed no difference between both phytophysiognomies (U=29.5, p>0.05) and presence of water bodies (U=48.5, p>0.05).

Figure 5
Non-metric Multidimensional Scaling of medium-large mammal community structure according to different phytophysiognomies (a) and presence of water bodies (b), recorded in the Serra de Santa Catarina, Northeast Brazil, between August 2012 and November 2014. The ANOSIM (one-way) analysis showed no difference between phytophysiognomies (R=0.1124, p>0.05) and a significant difference between the presence of water bodies (R=0.3907, p<0.05).

DISCUSSION

Medium-large mammalian species community

We documented a richness (S=12) similar to that obtained in studies performed in the Caatinga (Table 2), corresponding to 43% of total MLM species (S=28) known to the biome (Feijó & Langguth, 2013Feijó, A. & Langguth, A. 2013. Mamíferos de médio e grande porte do Nordeste do Brasil: distribuição e taxonomia, com descrição de novas espécies. Revista Nordestina de Biologia, 22: 3-225.), and close to that listed for neighboring municipalities of the SSC (see Table 2 for details). We confirmed the presence of Euphractus sexcinctus, Tamandua tetradactyla, Sapajus libidinosus, and Procyon cancrivorus, previously only reported by local informants. However, we failed to record Dasypus novemcinctus, Sylvilagus brasiliensis, Leopardus emiliae (formerly part of Leopardus tigrinus; sensuNascimento & Feijó, 2017Nascimento, F.O. & Feijó, A. 2017. Taxonomic revision of the tigrina Leopardus tigrinus (Schreber, 1775) species group (Carnivora, Felidae). Papéis Avulsos de Zoologia, 57(19): 231-264.), and Herpailurus yagouaroundi. The intense land-use change can be one of the main factors leading to the lack of some records. Dotta & Verdade (2007Dotta, G. & Verdade, L.M. 2007. Trophic categories in a mammal assemblage: diversity in an agricultural landscape. Biota Neotropica, 7(2): 287-292.) observed the predominance of diet generalist species in an anthropic landscape (matrix of pasture, eucalyptus, sugarcane, and native forest), contrasting with the reduction or extinguishing of specialized species. Additionally, Alves et al. (2016Alves, R.; Feijó, A.; Barboza, R.; Souto, W.; Fernandes-Ferreira, H.; Cordeiro-Estrela, P. & Langguth A. 2016. Game mammals of the Caatinga biome. Ethnobiology and Conservation, 5: 1-51. https://doi.org/10.15451/ec2016-7-5.5-1-51.
https://doi.org/10.15451/ec2016-7-5.5-1-...
) report that hunting also affects some species, even locally extinguishing or lowering the densities of some of them. That might have been preponderant to the absence of D. novemcinctus and S. brasiliensis, widely hunted and appreciated as bushmeat (Barboza et al., 2016Barboza, R.R.; Lopes, S.F.; Souto W.M.S; Fernandes-Ferreira, H. & Alves R.R.N. 2016. The role of game mammals as bushmeat in the Caatinga, Northeast Brazil. Ecology and Society, 21(2): 2. https://doi.org/10.5751/ES-08358-210202.
https://doi.org/10.5751/ES-08358-210202...
).

Table 2
Medium and large mammal richness comparison between sampling areas in the Caatinga. Legends: TS=Total richness; Cin=Cingulata; Pil=Pilosa; Pri=Primates; Lag=Lagomorpha; Car=Carnivora; Art=Artiodactyla; Rod=Rodentia. We did not accounted domestic species.

Although being specialized species, the virtual absence of L. emiliae and H. yagouaroundi may also be the result of the “ocelot effect”. According to this effect, the predation of small-sized prey by L. pardalis inhibits the presence and persistence of smaller felid species (Oliveira et al., 2010Oliveira, T.G.; Tortato, M.A.; Silveira, L.; Kasper, C.B.; Mazim, F.D.; Lucherini, M.; Jácomo, A.T.A.; Soares, J.B.G.; Marques, R.V. & Sunquist, M.E. 2010. Ocelot Ecology and its Effects on the Small-Felid Guild in the Lowland Neotropics. In: Macdonald, D.W. & Loveridge, A.J. Biology and conservation of wild felids. Oxford University Press. p. 559-580.). While ocelots do not suffer any negative effects from larger felids as a result of competitive exclusion. This may have been extended to C. thous that presented a single record (n=1), although being commonly abundant in the Caatinga (Delciellos, 2016Delciellos, A.C. 2016. Mammals of four Caatinga areas in northeastern Brazil: Inventory, species biology, and community structure. Check List, 12: 1-15. https://doi.org/10.15560/12.3.1916.
https://doi.org/10.15560/12.3.1916...
). Despite small felids being common to the Caatinga, habitat reduction certainly decrease prey densities that in turn drive the lack of such predators. Larger areas, on the other, undoubtedly benefits a higher number of predator species through the availability of different sized prey (see Schaller & Crawshaw, 1980Schaller, G.B. & Crawshaw, P.G. 1980. Movement pattern of jaguar. Biotropica, 12(3): 161-168.; Emmons, 1987Emmons, L.H. 1987. Feeding ecology of felids Comparative in a Neotropical rainforest. Behavioral Ecology and Sociobiology, 20(4): 271-283.).

In spite of the similarities of species richness to previous studies in the Caatinga, the area amount availability play a fundamental role. For instance, we recorded 12 species, comparing to 7-29 species recorded in protected areas in the states of Bahia, Ceará, and Piauí (see Table 2), probably due to the largest size of these areas and habitat heterogeneity they maintain. Therefore, habitat suitability and dynamic of population and community may be main drivers to those differences. Specific characteristics of study areas, such as the history of colonization and degradation may also have played an important role. Thus, differences in composition with respect to habitat heterogeneity are expected, as discussed below.

Effect of habitat type and presence of water bodies: preliminary and exploratory approaches

Probably the size of the study site (currently 112.1 km²) and its heterogeneity were decisive in the maintenance of the mammalian community. We considered habitat types (arboreal and shrubby) and conditions (water presence and absence) as a proxy for habitat heterogeneity and complexity, both (types and conditions) being paramount for the local abundance of MLM. The presence/absence of water bodies also showed significant differences, where sites with water bodies presented higher abundances. According to Gadelha-Neto et al. (2018Gadelha-Neto, P.C.; Costa, R.M.T. & Barbosa, M.R.V. 2018. Vegetação e Flora da Serra de Santa Catarina. In: Araujo, H.F.P. & Vieira-Filho, A.H. Biodiversidade na Serra de Santa Catarina - PB: uma proposta de criação do Parque Estadual Serra das Águas Sertanejas. João Pessoa, Governo do Estado da Paraíba, UFPB. p. 80-125.), arboreal phytophysiognomy (Seasonal Deciduous Forest) occurs mostly in the high slopes and tops of the SSC, with Rubiaceae plants (associated with humid microhabitats) comprising the second-largest diversity of local tree species. Such characteristics guarantee the maintenance of a more complex habitat, while the shrubby habitat act as a buffer zone, instead of pasture or agriculture landscape. The higher abundance of MLM in this buffer shrubby habitat may be a response to its larger size, whereas the arboreal phytophysiognomies represent a core environment, an important habitat to specialized species.

The water bodies are responsible for other effects on the diversity of mammals in the SSC, such as the maintenance of arboreal habitat, and proving to be a preponderant factor in the detection of MLM species. As a result, sampling sites with the presence of water recorded a different mammalian community compared to the sampling sites without water (Figs. 4 and 5). Even in tropical rain forests, wetter areas present a strong relationship between habitat structure, composition, and abundance of mammalian species (Williams et al., 2002Williams, S.E.; Marsh, H. & Winter, J. 2002. Spatial scale, species diversity, and habitat structure: small mammals in Australian Tropical Rain Forest. Ecology, 83(5): 1317-1329.). This result suggests that habitat structure (presence/absence of water) is even more crucial for the mammalian community in xeric habitats and/or with less resource availability, as in the SSC.

Habitat diversity also plays an important role in mammal richness, recording higher rates in more productive and humid habitats. This pattern was recorded in the Central Amazon (Tardio & Da Silveira, 2015Tardio, B.M.R. & Da Silveira, R. 2015. The role of forest structure and human occupation in structuring mammal assemblages in oligotrophic ecosystems of Central Amazonia. Austral Ecology, 40(3): 318-330.), Caatinga and associated environments (Freitas et al., 2005Freitas, R.R.; Rocha, P.L.B. & Simões-Lopes, P.C. 2005. Habitat structure and small mammals abundances in one semiarid landscape in the Brazilian Caatinga. Revista Brasileira de Zoologia, 22: 119-129.; Pereira & Geise, 2009Pereira, L.G. & Geise, L. 2009. Non-flying mammals of Chapada Diamantina (Bahia, Brazil). Biota Neotropica, 9: 185-196.; Bezerra et al., 2014Bezerra, A.M.R.; Lazar, A.; Bonvicino, C.R. & Cunha, A.S. 2014. Subsidies for a poorly known endemic semiarid biome of Brazil: non-volant mammals of an eastern region of Caatinga. Zoological Studies, 53: 1-16.; Rocha et al., 2015Rocha, P.A.; Ruiz-Esparza, J.; Beltrão-Mendes, R.; Ribeiro, A.S.; Campos, B.A.T.P. & Ferrari, S.F. 2015. Nonvolant mammals in habitats of the Caatinga scrub and cloud forest enclave at Serra da Guia, state of Sergipe. Revista Brasileira de Zoociências, 16: 93-103.; Delciellos, 2016Delciellos, A.C. 2016. Mammals of four Caatinga areas in northeastern Brazil: Inventory, species biology, and community structure. Check List, 12: 1-15. https://doi.org/10.15560/12.3.1916.
https://doi.org/10.15560/12.3.1916...
; Dias & Bocchiglieri, 2016Dias de, M.D. & Bocchiglieri, A. 2016. Riqueza e uso do habitat por mamíferos de médio e grande porte na Caatinga, nordeste do Brasil. Neotropical Biology and Conservation, 11: 38-46.), and the African savannah (Western, 1975Western, D. 1975. Water availability and its influence on the structure and dynamics of a savannah large mammal community. African Journal of Ecology, 13(3/4): 265-286.). The presence of water in xeric environments is so valuable that even artificial sources can change the geographical distribution of certain species (Owen-Smith, 1996Owen-Smith, N. 1996. Ecological guidelines for waterpoints in extensive protected areas. South African Journal of Wildlife Research, 26(4): 107-112.; James et al., 1999James, C.D.; Landsberg, J. & Morton, S.R. 1999. Provision of watering points in the Australian arid zone: a review of effects on biota. Journal of Arid Environment, 41: 87-121.), being particularly important to water-dependent species (compulsory drinkers: grazers and larger-sized species). Since they consume higher rates of resources with low water levels, the presence of water sources is mandatory for their occurrence (Owen-Smith, 1996Owen-Smith, N. 1996. Ecological guidelines for waterpoints in extensive protected areas. South African Journal of Wildlife Research, 26(4): 107-112.; Redfern et al., 2003Redfern, J.V.; Grant, R.; Biggs, H. & Getz, W.M. 2003. Surface-water constraints on herbivore foraging in the Kruger National Park, South Africa. Ecology, 84(8): 2092-2107.; Moreira-Ramírez et al., 2016Moreira-Ramírez, J.F.; Reyna-Hurtado, R.; Hidalgo-Mihart, M.; Naranjo, E.; Ribeiro, M.; Garcia-Anleu, R.; Mérida, M. & Ponce-Santizo, G. 2016. Importance of waterholes for white-lipped peccary (Tayassu pecari) in the Selva Maya, Guatemala. Therya, 7: 51-64.).

Mammals from Caatinga are physiologically less adapted to hydric stress (see Mares et al., 1985Mares, M.A.; Willing, M.R. & Lacher, T.E. 1985. The Brazilian Caatinga in South American zoogeography: tropical mammals in a dry region. Journal of Biogeography, 12: 57-69.) highlighting the requirement for regular water sources. However, the presence of water affects mammals less as the remaining forest increases. In Serra da Capivara National Park (Parque Nacional Serra da Capivara - PNSC; 130,000 ha) mammals were not affected by distance from water sources (Wolff, 2001Wolff, F. 2001. Vertebrate ecology in Caatinga: A. Distribution of wildlife in relation to water. B. Diet of pumas (Puma concolor) and relative abundance of felids. (Doctoral Thesis). University of Missouri.). The same was not observed in the Serra das Almas Private Natural Heritage Reserve (Reserva Particular do Patrimônio Natural Serra das Almas - RPPN Serra das Almas; 5,800 ha) (Dias et al., 2017Dias, D.D.M.; Guedes, P.G., Silva, S.S.P. & Sena, L.M.M. 2017. Diversity of nonvolant mammals in a Caatinga area in northeastern Brazil. Neotropical Biology and Conservation, 12(3): 200-208.). Notwithstanding, the later authors did not evaluate the water effect on mammalian abundance. The maintenance of higher quality habitats in the PNSC and RPPN Serra das Almas, due to their large size, guarantees a lower effect of drought events. It certainly decreases dependence on water bodies. Thus, the consequences of the presence of water seem to exert a strong influence on richness and abundance as forest remnants decrease in size, as observed in the present study. Additionally, these habitat characteristics may be even more important during prolonged droughts. Further investigations may address better attention to those characteristics (habitat type and condition) and their effect on mammalian community along the Caatinga biome.

Threats and conservation

Regarding the species richness, the SSC exhibit an intermediate conservation status. The SSC presents both MLM species that are common and tolerant to anthropic pressure (e.g., Callithrix jacchus, Cerdocyon thous), as well as rare and lower tolerant to anthropization (e.g., Puma concolor). We highlight the presence of Kerodon rupestris (endemic to Caatinga - Gutiérrez & Marinho-Filho, 2017Gutiérrez, E. & Marinho-Filho, J. 2017. The mammalian faunas endemic to the Cerrado and the Caatinga. Zookeys, 644: 105-157. https://doi.org/10.3897/zookeys.644.10827.
https://doi.org/10.3897/zookeys.644.1082...
), considered to be threatened with extinction (see Table 2). The recent review of threatened species in Brazil (“National red list”, MMA, 2022Ministério do Meio Ambiente (MMA). 2022. Portaria № 300, de 13 de dezembro de 2022. Reconhece a Lista Nacional de Espécies Ameaçadas de Extinção, conforme Anexo I desta presente Portaria. Diário Oficial da União, Edição 234, Seção 1, p. 75, 2022.) does not consider regional or state contexts, removing sensitive species such as Puma concolor. However, these species deal with regional threats, facing a reduction in local populations, if not local extinctions. In this sense, State red lists would deal with such local or regional contexts for sensitive species, being an important outcome for local policy.

The species found in the SSC are commonly subjected to hunting. Euphractus sexcinctus, K. rupestris, and S. gouazoubira are possibly the most affected species by the hunting activity, usually as bushmeat. Traps, standing points and baiting points (NFC and BATPC, pers. obs.) confirm the hunting activity along the SSC. The subsistence may be the main purposes. However, even species with high reproductive rates as the K. rupestris, is facing local extinction due to its overexploitation (Alves et al., 2016Alves, R.; Feijó, A.; Barboza, R.; Souto, W.; Fernandes-Ferreira, H.; Cordeiro-Estrela, P. & Langguth A. 2016. Game mammals of the Caatinga biome. Ethnobiology and Conservation, 5: 1-51. https://doi.org/10.15451/ec2016-7-5.5-1-51.
https://doi.org/10.15451/ec2016-7-5.5-1-...
; Barboza et al., 2016Barboza, R.R.; Lopes, S.F.; Souto W.M.S; Fernandes-Ferreira, H. & Alves R.R.N. 2016. The role of game mammals as bushmeat in the Caatinga, Northeast Brazil. Ecology and Society, 21(2): 2. https://doi.org/10.5751/ES-08358-210202.
https://doi.org/10.5751/ES-08358-210202...
). Hunting also directly affects the Puma concolor due to conflicts with humans in order to avoid livestock loss (mainly goats). Indirectly, hunting decreases the number of prey, mainly medium-sized mammals (Carvalho-Jr. & Morato, 2013Carvalho-Jr., E.A.R. & Morato, R.G. 2013. Factors affecting big cat hunting in Brazilian protected areas. Tropical Conservation Science, 6: 303-310.; Michalski et al., 2006Michalski, F.; Boulhosa, R.L.P.; Faria, A. & Peres, C.A. 2006. Human-wildlife conflicts in a fragmented Amazonian forest landscape: Determinants of large felid depredation on livestock. Animal Conservation, 9(2): 179-188.). The excessive withdrawal of specimens from the nature is one of the most important threats to the wildlife (Dirzo et al., 2014Dirzo, R.; Young, H.S.; Galetti, M.; Ceballos, G.; Isaac, N.J.B. & Collen, B. 2014. Defaunation in the Antrhopocene. Science, 80(6195): 401-406.). In the Neotropics, hunting is usually performed in an impactful and unsustainable manner (e.g.,Alvard et al., 1997Alvard, M.S.; Robinson, J.G.; Redford, K.H. & Kaplan, H. 1997. The sustainability of subsistence hunting in the Neotropics. Conservation Biology, 11(4): 977-982. https://doi.org/10.1046/j.1523-1739.1997.96047.x.
https://doi.org/10.1046/j.1523-1739.1997...
; Nogueira & Nogueira-Filho, 2011Nogueira, S.S.C. & Nogueira-Filho, S.L.G. 2011. Wildlife farming: An alternative to unsustainable hunting and deforestation in Neotropical forests? Biodiversity and Conservation, 20(7): 1385-1397.), even in Caatinga MLM (Barboza et al., 2016Barboza, R.R.; Lopes, S.F.; Souto W.M.S; Fernandes-Ferreira, H. & Alves R.R.N. 2016. The role of game mammals as bushmeat in the Caatinga, Northeast Brazil. Ecology and Society, 21(2): 2. https://doi.org/10.5751/ES-08358-210202.
https://doi.org/10.5751/ES-08358-210202...
). This makes the Caatinga historically the most impacted in Brazil due to hunting.

Followed by hunting, habitat reduction and fragmentation are the main drive to the biodiversity loss (Chiarello et al., 2008Chiarello, A.G.; Aguilar, L.M.D.S.; Cerqueira, R.; De Melo, F.R.; Rodrigues, F.H.G. & Da Silva, V.M.F. 2008. Mamíferos ameaçados de extinção no Brasil. In: Livro vermelho da fauna brasileira ameaçada de extinção, Brasília, Ministério do Meio Ambiente. 203p.; ICMBio, 2018Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). 2018. Livro Vermelho da Fauna Brasileira Ameaçada de Extinção: Volume II - Mamíferos. In: Instituto Chico Mendes de Conservação da Biodiversidade. Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. Brasília, ICMBio. 622p.). The conservation measurements to the local diversity of the SSC, therefore, should consider not only the protection of the forest remnant, but the nearby forest remnants. The establishment of forest corridors associated with riparian forest, besides being a largely used strategy, allows the supply of the perennial condition of small streams even if they get far from the SSC. This strategy allows mammals and other animal species to travel between forest remnants. It also guarantees a decrease in the effects of prolonged droughts on the water reservoirs supply located in the SSC surroundings. Sustaining local human populations and their diverse activities. The creation and maintenance of artificial water sources such as dam along the SSC can also be an important strategy to maintain the local mammal species or even other groups of animals. Artificial water spots are utilized as management measures of protected areas (PA) in Africa and Australia. This strategic spots guarantee water source during prolonged drought periods, besides being touristic points (see Owen-Smith, 1996Owen-Smith, N. 1996. Ecological guidelines for waterpoints in extensive protected areas. South African Journal of Wildlife Research, 26(4): 107-112.; James et al., 1999James, C.D.; Landsberg, J. & Morton, S.R. 1999. Provision of watering points in the Australian arid zone: a review of effects on biota. Journal of Arid Environment, 41: 87-121.; Redfern et al., 2003Redfern, J.V.; Grant, R.; Biggs, H. & Getz, W.M. 2003. Surface-water constraints on herbivore foraging in the Kruger National Park, South Africa. Ecology, 84(8): 2092-2107.).

CONCLUSIONS

Our results highlight the importance of setting the camera-traps both near water bodies and through different habitat types. That guarantees the sampling of a higher number of species in a small time-effort, in preliminary, or in rapid mammalian survey/assessment. Besides, it is possible to evaluate the effect of habitat type and water presence in the distribution of mammalian fauna throughout the Caatinga habitats.

We observed that habitat type (phytophysiognomy) is an important variable affecting the distribution, composition, and abundance of mammals in xeric environment, corroborating previous studies. We highlights the need of maintenance of large forest remnants of the Caatinga, especially those with large arboreal habitats. The present study also highlights the significance of water sources or more humid habitats to the maintenance of MLM fauna throughout the Caatinga. Particularly when forest remnants are reduced. Which means, whereas the forest remnants get smaller the water presence becomes a preponderant factor in the presence and abundance of mammals in xeric environments. That emphasizes the importance of protection of Caatinga areas such as the Serra de Santa Catarina. They are responsible for the maintenance of mammal diversity in a biome with a lack of protected areas. The conservation of the SSC brings as a consequence the maintenance of the local hydric resources. An important resource for local populations and their economic activities, mainly in semiarid environments.

In time, it is important to consider that factors such as fragment size and hunting can also exert a strong influence over the maintenance of those species, therefore, they should be considered as a variable in further studies. Future researches may also consider the investigation of the effect of arboreal and shrubby environments in the context of core and buffer conditions, as pointed by the present results.

ACKNOWLEDGEMENTS

We are thankful for the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for research fellow to RB-M (150123/2018-3), and CAPES for PNPD research fellow to RB-M (88887.320996/2019-00) and BATPC. We also thankful to Dr. Helder Farias Pereira de Araújo for the invitation to join this project during whose development the present data was obtained. We are also in debt with Thiago Cezar Farias da Silva, who provided logistical support in collaboration with de Superintendência de Administração do Meio Ambiente (SUDEMA).

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  • FUNDING INFORMATION:

    Tropical Forest Conservation Act (TFCA) in association with the Fundo Brasileiro para a Diversidade (FUNBIO) (Project 3; 01/2011) funded the project “Potencialidades para Criação de Unidade de Conservação de Proteção Integral na Serra de Santa Catarina - Paraíba”. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001”.
  • Published with the financial support of the "Programa de Apoio às Publicações Científicas da Universidade de São Paulo"

Edited by

Edited by:

Luís Fábio Silveira.

Publication Dates

  • Publication in this collection
    22 Sept 2023
  • Date of issue
    2023

History

  • Received
    14 July 2022
  • Accepted
    30 June 2023
  • Published
    01 Aug 2023
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