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Can the type and placement of traps influence the capturability of marsupials according to their body weight? A case study with Didelphis albiventris and Gracilinanus agilis in central Brazil

ABSTRACT

Body weight and vertical stratum utilization are important functional characteristics of species. Several studies have explored the capture success of different traps. These studies, however, did not explore how trappability is influenced by body weight. Here, we investigated the relationship between the weight of marsupial species caught in traps with trap type (wire cage and Sherman) and trap placement (ground and understory). For this we used data from Didelphis albiventris Lund, 1840 (n = 127; 75-958 g) and Gracilinanus agilis (Burmeister, 1854) (n = 327; 8.5-46 g) captured in semideciduous forest fragments in central Brazil. The results show that heaviest individuals of D. albiventris (391.01 ± 197.57 g) were captured more often by wire cage traps, regardless of trap placement. In contrast, G. agilis was trapped at similar rates regardless of weight, trap type or trap placement. We conclude that wire cage traps are more efficient at catching large marsupials weighing more than 300 g on average. Furthermore, the size of the individuals captured is not influenced by where the trap is placed (ground or understory). These findings contribute to a better understanding of the natural history and trappability of Neotropical marsupials.

KEY WORDS:
Ground; marsupials; sherman trap; understory; wire cage

Marsupials (Didelphimorphia), are a diverse group of mammals with wide distribution across all the American continent, inhabiting various vegetation types (Gardner 2008Gardner AL (2008) Mammals of South America: marsupials, xenarthrans, sherews, and bats. The University of Chicago Press, Chicago, 669 pp., Voss and Jansa 2021Voss RS, Jansa SA (2021) Opossums: an adaptive radiation of new world marsupials. Johns Hopkins University Press, Baltimore, 313 pp.). Their size (ranging from 10 to 3000 g), diet, habitat use, and type of locomotion (terrestrial, semiaquatic, scansorial, and arboreal) vary greatly (Gardner 2008, Voss and Jansa 2021), making them excellent models for ecological studies. To access the full functional and phylogenetic diversity of marsupials, different collecting campaigns, using different types and placement of traps, have been conducted in different Brazilian biomes (Lambert et al. 2005Lambert TD, Malcolm JR, Zimmerman BL (2005) Variation in small mammal species richness by trap height and trap type in southeastern 419 Amazonia. Journal of Mammalogy 86: 982-990. https://doi.org/10.1644/1545-1542(2005)86[982:VISMSR]2.0.CO;2
https://doi.org/10.1644/1545-1542(2005)8...
, Astúa et al. 2006Astúa D, Moura RT, Grelle CEV, Fonseca MT (2006) Influence of baits, trap type and position for small mammal capture in a Brazilian lowland Atlantic Forest. Boletim do Museu de Biologia Mello Leitão 19: 31-44., Umetsu et al. 2006Umetsu F, Naxara L, Pardini R (2006) Evaluating the efficiency of pitfall traps for sampling small mammals in the Neotropics. Journal of Mammalogy 87: 757-765. https://doi.org/10.1644/05-MAMM-A-285R2.1
https://doi.org/10.1644/05-MAMM-A-285R2....
, Cáceres et al. 2011Caceres NC, Nápoli RP, Hannibal W (2011) Differential trapping success for small mammals using pitfall and standard cage traps in a woodland savannah region of southwestern Brazil. Mammalia 75: 45-42. https://doi.org/10.1515/mamm.2010.069
https://doi.org/10.1515/mamm.2010.069...
, Santos-Filho et al. 2015Santos-Filho M, Lázari PR, Souza CPF, Canale GR (2015) Trap efficiency evaluation for small mammals in the southern Amazon. Acta Amazonica 45(2): 187-194. https://doi.org/10.1590/1809-4392201401953
https://doi.org/10.1590/1809-43922014019...
, Bovendorp et al. 2017Bovendorp RS, McCleery RA, Galetti M (2017) Optimising sampling methods for small mammals communities in Neotropical rainforests. Mammal Review 47(2): 148-158. https://doi.org/10.1111/mam.12088
https://doi.org/10.1111/mam.12088...
, Figueiredo et al. 2021Figueiredo VV, Cunha NL, Morais AR, Terribile LC, Hannibal W (2021) The importance of sampling methods and landscape variation on explaining small mammal communities in a Neotropical ecotone region. Mammal Research 66: 301-312. https://doi.org/10.1007/s13364-021-00558-7
https://doi.org/10.1007/s13364-021-00558...
).

Several types of traps have been commonly used to capture small mammals, including pitfall traps, Sherman traps, and wire cage traps (Bovendorp et al. 2017Bovendorp RS, McCleery RA, Galetti M (2017) Optimising sampling methods for small mammals communities in Neotropical rainforests. Mammal Review 47(2): 148-158. https://doi.org/10.1111/mam.12088
https://doi.org/10.1111/mam.12088...
). These studies have focused on evaluating the effects of trap type and placement (either on the ground or in the understory) on various parameters such as abundance, species richness, composition, and capture success (Lambert et al. 2005Lambert TD, Malcolm JR, Zimmerman BL (2005) Variation in small mammal species richness by trap height and trap type in southeastern 419 Amazonia. Journal of Mammalogy 86: 982-990. https://doi.org/10.1644/1545-1542(2005)86[982:VISMSR]2.0.CO;2
https://doi.org/10.1644/1545-1542(2005)8...
, Astúa et al. 2006Astúa D, Moura RT, Grelle CEV, Fonseca MT (2006) Influence of baits, trap type and position for small mammal capture in a Brazilian lowland Atlantic Forest. Boletim do Museu de Biologia Mello Leitão 19: 31-44., Umetsu et al. 2006Umetsu F, Naxara L, Pardini R (2006) Evaluating the efficiency of pitfall traps for sampling small mammals in the Neotropics. Journal of Mammalogy 87: 757-765. https://doi.org/10.1644/05-MAMM-A-285R2.1
https://doi.org/10.1644/05-MAMM-A-285R2....
, Cáceres et al. 2011Caceres NC, Nápoli RP, Hannibal W (2011) Differential trapping success for small mammals using pitfall and standard cage traps in a woodland savannah region of southwestern Brazil. Mammalia 75: 45-42. https://doi.org/10.1515/mamm.2010.069
https://doi.org/10.1515/mamm.2010.069...
, Santos-Filho et al. 2015Santos-Filho M, Lázari PR, Souza CPF, Canale GR (2015) Trap efficiency evaluation for small mammals in the southern Amazon. Acta Amazonica 45(2): 187-194. https://doi.org/10.1590/1809-4392201401953
https://doi.org/10.1590/1809-43922014019...
, Bovendorp et al. 2017, Figueiredo et al. 2021Figueiredo VV, Cunha NL, Morais AR, Terribile LC, Hannibal W (2021) The importance of sampling methods and landscape variation on explaining small mammal communities in a Neotropical ecotone region. Mammal Research 66: 301-312. https://doi.org/10.1007/s13364-021-00558-7
https://doi.org/10.1007/s13364-021-00558...
). Some studies have also examined the relationship between the type of trap and the weight of the body of the captured individuals (Lyra-Jorge and Pivello 2001Lyra-Jorge MC, Pivello VR (2001) Combining live trap and pitfall to survey terrestrial small mammals in savanna and forest habitats, in Brazil. Mammalia 65: 524-530., Astúa et al. 2006Astúa D, Moura RT, Grelle CEV, Fonseca MT (2006) Influence of baits, trap type and position for small mammal capture in a Brazilian lowland Atlantic Forest. Boletim do Museu de Biologia Mello Leitão 19: 31-44., Nicolas and Colyn 2006Nicolas V, Colyn M (2006) Relative efficiency of three types of small mammal traps in an African rainforest. Belgian Journal of Zooloology 136: 107-111., Umetsu et al. 2006Umetsu F, Naxara L, Pardini R (2006) Evaluating the efficiency of pitfall traps for sampling small mammals in the Neotropics. Journal of Mammalogy 87: 757-765. https://doi.org/10.1644/05-MAMM-A-285R2.1
https://doi.org/10.1644/05-MAMM-A-285R2....
, Cáceres et al. 2011Caceres NC, Nápoli RP, Hannibal W (2011) Differential trapping success for small mammals using pitfall and standard cage traps in a woodland savannah region of southwestern Brazil. Mammalia 75: 45-42. https://doi.org/10.1515/mamm.2010.069
https://doi.org/10.1515/mamm.2010.069...
, Hice and Velazco 2013Hice CL, Velazco PM (2013) Relative effectiveness of several bait and trap types for assessing terrestrial small mammal communities in neotropical rainforest. Occasional Papers 316: 1-15.). A few studies have investigated the interaction between trap type and placement (Figueiredo et al. 2021Figueiredo VV, Cunha NL, Morais AR, Terribile LC, Hannibal W (2021) The importance of sampling methods and landscape variation on explaining small mammal communities in a Neotropical ecotone region. Mammal Research 66: 301-312. https://doi.org/10.1007/s13364-021-00558-7
https://doi.org/10.1007/s13364-021-00558...
) and trappability, and trap type and placement and body weight. It has been observed that wire cage traps tend to capture larger animals (> 250 g) compared to Sherman traps (Astúa et al. 2006Astúa D, Moura RT, Grelle CEV, Fonseca MT (2006) Influence of baits, trap type and position for small mammal capture in a Brazilian lowland Atlantic Forest. Boletim do Museu de Biologia Mello Leitão 19: 31-44., Cáceres et al. 2011Caceres NC, Nápoli RP, Hannibal W (2011) Differential trapping success for small mammals using pitfall and standard cage traps in a woodland savannah region of southwestern Brazil. Mammalia 75: 45-42. https://doi.org/10.1515/mamm.2010.069
https://doi.org/10.1515/mamm.2010.069...
, Hice and Velazco 2013Hice CL, Velazco PM (2013) Relative effectiveness of several bait and trap types for assessing terrestrial small mammal communities in neotropical rainforest. Occasional Papers 316: 1-15.), and lighter individuals, even those belonging to relatively large species, are more effectively captured in Sherman traps than heavier individuals (Nicolas and Colyn 2006Nicolas V, Colyn M (2006) Relative efficiency of three types of small mammal traps in an African rainforest. Belgian Journal of Zooloology 136: 107-111.).

In this study, we investigate whether the type of trap (Sherman or wire cage) and where the trap is placed (placement on the ground or in the understory) influence the rate of capture of Didelphis albiventris Lund, 1840 and Gracilinanus agilis (Burmeister, 1854), and whether the weight of the body the individuals captured correlates with those two variables. Our hypothesis was that larger animals, particularly D. albiventris, which is a medium-sized scansorial marsupial, would be captured more frequently by wire cage traps regardless of trap placement, while smaller animals, including G. agilis, a scansorial species (Vieira and Camargo 2012Vieira EM, Camargo NF (2012) Uso do espaço vertical por marsupiais brasileiros. In: Cáceres NC (Ed.) Os marsupiais do Brasil: biologia, ecologia e conservação. Editora da UFMS, Campo Grande, 348-366.), would be captured more frequently by Sherman traps placed in the understory. Furthermore, we hypothesized that larger individuals, such as adults, of both D. albiventris and G. agilis, spend more time on the ground and hence will be captured more frequently there (Cunha and Vieira 2005Cunha AA, Vieira MV (2005) Age, season, and arboreal movements of the opossum Didelphis aurita in an Atlantic rain forest of Brazil. Acta Theriol 50: 551-560. https://doi.org/10.1007/BF03192648
https://doi.org/10.1007/BF03192648...
). Our study aims to provide insights into the factors influencing animal capture using traps in natural environments, contributing to natural history of marsupials.

We surveyed small mammals captured in 44 trap grids located in semideciduous forest fragments in southern Goiás, central Brazil. These fragments were either connected or isolated from gallery forests. In 2015, we sampled 24 grids from January to June, and re-sampled them from July to December. The remaining 20 grids were sampled in 2020 and re-sampled in 2021 and 2022, with quarterly captures (5-grids per quarter). In the case of the first 24 grids (2015), we established 16 capture stations that were distributed across four transects. In the case of the other 20 grids (2020-2022), we used 10 capture stations, distributed across two transects. Each capture station was spaced 15 m apart from the others and consisted of two traps (one Sherman [25 x 8 x 9 cm] and one-wire cage [30 x 13 x 13 cm]) set on the ground and in the understory (1.5 to 2 m high), alternately. This approach allowed us to standardize the number of Sherman traps and wire cages on the ground and in the understory for each trap grid. The traps were active for five to seven nights, resulting in a total effort of 4,588 trap-nights per trap type (Sherman and wire cage) and placement (ground and understory), totaling 18,352 trap-nights.

To investigate the effect of trap type (Sherman and wire cage) as the explanatory variable 1, interacting with trap placement (ground and understory) as the explanatory variable 2, on the response variable of body weight, we performed a Factorial Analysis of Variance (ANOVA) using the ‘aov’ function in the R program (R Core Team 2021R Core Team (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available online at: https://www.R-project.org/
https://www.R-project.org/...
). The model formula used was ‘var.response ~ var.explanatory1 * var.explanatory2’.

We captured 80 individuals of D. albiventris (n = 127 captures distributed in trap type [24 in Sherman and 103 in wire-cage traps] and trap placement [102 on the ground and 25 in the understory] captures) and 210 individuals of G. agilis (n = 327 captures distributed in trap type [180 in Sherman and 147 in wire cage traps] and trap placement [74 on the ground and 253 in the understory] captures) in the fragmented landscape of southern Goiás. The body weight of D. albiventris ranged from 75 g (a female captured in a Sherman trap in the understory) to 958 g (a male captured in a wire cage trap on the ground). The heaviest D. albiventris (mean = 391.01 ± 197.57 standard deviation) were captured in greater numbers by wire cage traps, regardless of the placement of the trap (Table 1, Fig. 1), a result that is statistically significant (F = 9.335, p = 0.003). On the other hand, the body weight of G. agilis in traps ranged from 8.5 g (one male captured in Sherman trap in the understory) to 46 g (1 male captured in Sherman trap in the understory), and was not significantly correlated with trap type or placement, or their interaction (Table 1, Fig. 1).

Figure 1
Mean and standard deviation of bodied weight (g) for (A) Didelphis albiventris and (B) Gracilinanus agilis captured in semi-deciduous forest fragments in central Brazil. Silhouette according PhyloPic - free silhouette images of organisms, version 2.0 (https://www.phylopic.org/).

Table 1
Factorial ANOVA for association trap type, trap position and the interaction between these variables with the weight average of two marsupials captured in semi-deciduous forest fragments in central Brazil. The significant relation (p < 0.05) is highlight in bold.

Our hypothesis was partially supported by our results. Heavier D. albiventris individuals were captured using wire cage traps, while lighter individuals were captured using Sherman traps, regardless of trap placement. In the case of G. agilis, the type and placement of the traps did not significantly affect capturability variation by weight, although on average, heavier animals were more often captured on the ground. In the Atlantic Forest fragments, Sherman traps captured lighter weight marsupials (average weight = 60.23 ± 45.55 g SD) compared to wire cage traps (average weight = 267.48 ± 236.05) of the Tomahawk type (Astúa et al. 2006Astúa D, Moura RT, Grelle CEV, Fonseca MT (2006) Influence of baits, trap type and position for small mammal capture in a Brazilian lowland Atlantic Forest. Boletim do Museu de Biologia Mello Leitão 19: 31-44.). This pattern had been previously observed in small mammals in the Brazilian Cerrado (Cáceres et al. 2011) and in the Peruvian Amazon, where individuals with body weight >249 g were frequently captured using Tomahawk traps (Hice and Velazco 2013Hice CL, Velazco PM (2013) Relative effectiveness of several bait and trap types for assessing terrestrial small mammal communities in neotropical rainforest. Occasional Papers 316: 1-15.). Our wire cage traps are slightly larger (30 x 13 x 13 cm) than our Sherman traps (25 x 8 x 9 cm), providing more space for capturing larger individuals. According to Astúa et al. (2006Astúa D, Moura RT, Grelle CEV, Fonseca MT (2006) Influence of baits, trap type and position for small mammal capture in a Brazilian lowland Atlantic Forest. Boletim do Museu de Biologia Mello Leitão 19: 31-44.), larger species may find alternative ways to access the bait if the trap opening is too small, resulting in trap deactivation without capture, while smaller species may consume the bait without being caught in larger and less sensitive traps.

The placement of traps was not correlated with the body weight of the two species investigated. Our expectation was that heavier individuals, typically adults, would have better access to all three dimensions of the forest, regardless of their scansorial or arboreal habits, and would be captured on the ground. On the other hand, lighter individuals would seek protection against terrestrial predators in the upper strata of the forest, making the understory their common habitat (Cunha and Vieira 2005Cunha AA, Vieira MV (2005) Age, season, and arboreal movements of the opossum Didelphis aurita in an Atlantic rain forest of Brazil. Acta Theriol 50: 551-560. https://doi.org/10.1007/BF03192648
https://doi.org/10.1007/BF03192648...
, Vieira and Camargo 2012Vieira EM, Camargo NF (2012) Uso do espaço vertical por marsupiais brasileiros. In: Cáceres NC (Ed.) Os marsupiais do Brasil: biologia, ecologia e conservação. Editora da UFMS, Campo Grande, 348-366.). Additionally, young and sub-adult individuals of D. aurita tend to be lighter but have relatively larger legs and claws, making them better adapted for tree climbing and enabling them to make better use of the upper stratum (Vieira 1997Vieira MV (1997) Body size and form in two neotropical marsupials, Didelphis aurita and Philander opossum (Marsupialia: Didelphidae). Mammalia 61(2): 245-254. https://doi.org/10.1515/mamm.1997.61.2.245
https://doi.org/10.1515/mamm.1997.61.2.2...
). However, the placement of the traps did impact the number of captures, with D. albiventris being more frequently captured on the ground, while G. agilis was captured more often in the understory (Figueiredo et al. 2021Figueiredo VV, Cunha NL, Morais AR, Terribile LC, Hannibal W (2021) The importance of sampling methods and landscape variation on explaining small mammal communities in a Neotropical ecotone region. Mammal Research 66: 301-312. https://doi.org/10.1007/s13364-021-00558-7
https://doi.org/10.1007/s13364-021-00558...
), which was expected considering the locomotor habits and vertical stratification patterns of these species (Vieira and Camargo 2012Vieira EM, Camargo NF (2012) Uso do espaço vertical por marsupiais brasileiros. In: Cáceres NC (Ed.) Os marsupiais do Brasil: biologia, ecologia e conservação. Editora da UFMS, Campo Grande, 348-366.).

The correlation between body weight and trap type and trap placement has been poorly documented in the scientific literature, especially when focusing on intraspecific patterns. In this study, we found that wire cage traps tend to capture heaver D. albiventris individuals when compared to Sherman traps. However, the capture of smaller species such as G. agilis was not influenced by trap type, trap placement or body weight. The utilization of different vertical strata by each species may be influenced by intrinsic factors, such as sex, age, and body size, as well as extrinsic factors, including resource availability, predator presence, and seasonality.

ACKNOWLEDGEMENTS

We are thankful to the members of the Laboratory of Ecology and Biogeography of Mammals for their help in the field. The Universidade Estadual de Goiás and the city hall of Quirinópolis provided logistical support of the research. The Universidade Estadual de Goiás for the scholarship granted to CA and financial support through Pró-Programas (UEG 04/2021). The Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship granted to ACBD and HWPC, and for financial support through PROAP (CAPES 0553/2021, process 88881.652040/2021-01). We also thank the two anonymous reviewers that substantial contribution on reviewing this manuscript. WH is Conselho Nacional de Desenvolvimento Científico e Tecnológico research fellow (CNPq, protocol 0817589137277209) in Brazil.

LITERATURE CITED

  • Astúa D, Moura RT, Grelle CEV, Fonseca MT (2006) Influence of baits, trap type and position for small mammal capture in a Brazilian lowland Atlantic Forest. Boletim do Museu de Biologia Mello Leitão 19: 31-44.
  • Bovendorp RS, McCleery RA, Galetti M (2017) Optimising sampling methods for small mammals communities in Neotropical rainforests. Mammal Review 47(2): 148-158. https://doi.org/10.1111/mam.12088
    » https://doi.org/10.1111/mam.12088
  • Caceres NC, Nápoli RP, Hannibal W (2011) Differential trapping success for small mammals using pitfall and standard cage traps in a woodland savannah region of southwestern Brazil. Mammalia 75: 45-42. https://doi.org/10.1515/mamm.2010.069
    » https://doi.org/10.1515/mamm.2010.069
  • Cunha AA, Vieira MV (2005) Age, season, and arboreal movements of the opossum Didelphis aurita in an Atlantic rain forest of Brazil. Acta Theriol 50: 551-560. https://doi.org/10.1007/BF03192648
    » https://doi.org/10.1007/BF03192648
  • Figueiredo VV, Cunha NL, Morais AR, Terribile LC, Hannibal W (2021) The importance of sampling methods and landscape variation on explaining small mammal communities in a Neotropical ecotone region. Mammal Research 66: 301-312. https://doi.org/10.1007/s13364-021-00558-7
    » https://doi.org/10.1007/s13364-021-00558-7
  • Gardner AL (2008) Mammals of South America: marsupials, xenarthrans, sherews, and bats. The University of Chicago Press, Chicago, 669 pp.
  • Hice CL, Velazco PM (2013) Relative effectiveness of several bait and trap types for assessing terrestrial small mammal communities in neotropical rainforest. Occasional Papers 316: 1-15.
  • Lambert TD, Malcolm JR, Zimmerman BL (2005) Variation in small mammal species richness by trap height and trap type in southeastern 419 Amazonia. Journal of Mammalogy 86: 982-990. https://doi.org/10.1644/1545-1542(2005)86[982:VISMSR]2.0.CO;2
    » https://doi.org/10.1644/1545-1542(2005)86[982:VISMSR]2.0.CO;2
  • Lyra-Jorge MC, Pivello VR (2001) Combining live trap and pitfall to survey terrestrial small mammals in savanna and forest habitats, in Brazil. Mammalia 65: 524-530.
  • Nicolas V, Colyn M (2006) Relative efficiency of three types of small mammal traps in an African rainforest. Belgian Journal of Zooloology 136: 107-111.
  • R Core Team (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available online at: https://www.R-project.org/
    » https://www.R-project.org/
  • Santos-Filho M, Lázari PR, Souza CPF, Canale GR (2015) Trap efficiency evaluation for small mammals in the southern Amazon. Acta Amazonica 45(2): 187-194. https://doi.org/10.1590/1809-4392201401953
    » https://doi.org/10.1590/1809-4392201401953
  • Umetsu F, Naxara L, Pardini R (2006) Evaluating the efficiency of pitfall traps for sampling small mammals in the Neotropics. Journal of Mammalogy 87: 757-765. https://doi.org/10.1644/05-MAMM-A-285R2.1
    » https://doi.org/10.1644/05-MAMM-A-285R2.1
  • Vieira MV (1997) Body size and form in two neotropical marsupials, Didelphis aurita and Philander opossum (Marsupialia: Didelphidae). Mammalia 61(2): 245-254. https://doi.org/10.1515/mamm.1997.61.2.245
    » https://doi.org/10.1515/mamm.1997.61.2.245
  • Vieira EM, Camargo NF (2012) Uso do espaço vertical por marsupiais brasileiros. In: Cáceres NC (Ed.) Os marsupiais do Brasil: biologia, ecologia e conservação. Editora da UFMS, Campo Grande, 348-366.
  • Voss RS, Jansa SA (2021) Opossums: an adaptive radiation of new world marsupials. Johns Hopkins University Press, Baltimore, 313 pp.

ADDITIONAL NOTES

  • ZooBank register

    https://zoobank.org/64F750C9-627A-4C3A-BDC2-22ACB75E9A19
  • How to cite this article

    Claro HWP, Bernardes-Dias AC, Alves C, Hannibal W (2023) Can the type and placement of traps influence the capturability of marsupials according to their body weight? A case study with Didelphis albiventris and Gracilinanus agilis in central Brazil. Zoologia 41: e23030. https://doi.org/10.1590/S1984-4689.v41.e23030
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    Sociedade Brasileira de Zoologia at Scientific Electronic Library Online (https://www.scielo.br/zool)

Edited by

Editorial responsibility

Guilherme S.T. Garbino

Publication Dates

  • Publication in this collection
    19 Jan 2024
  • Date of issue
    2024

History

  • Received
    21 June 2023
  • Accepted
    27 Aug 2023
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