Intra and inter-monkey transmission of bacteria in wild black capuchins monkeys (Sapajus nigritus): a preliminary study

T. T. Grassotti D. A. Zvoboda L. F. X. Costa F. D. P. Christiano M. B. Mann P. G. C. Wagner A. A. S. Campos J. Frazzon A. P. G. Frazzon About the authors

Black capuchin monkeys (Sapajus nigritus) are characterized by presence of robust capuchin monkeys, which have adornments or tufts on the head. Monkeys live in a social structure involves hierarchies of dominance between males and females, which results in different behaviors, such as agonistic, affiliative, and cooperative (Valença-Silva et al., 2014VALENÇA-SILVA, G., MACIEL, F.G., ZAGANINI, R.L., LUCINDO, A.S., CARAMASCHI, S. and PAULA, H.M.G., 2014. Reporting social behaviours of mixed-species troops formed by Callithrix jacchus and Callithrix penicillata (Primate, Callitrichidae). Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 74, no. 3, pp. 607-611. http://dx.doi.org/10.1590/bjb.2014.0091. PMid:25296209.
http://dx.doi.org/10.1590/bjb.2014.0091...
; Back et al., 2019BACK, J.P., SUZIN, A. and AGUIAR, L.M., 2019. Activity budget and social behavior of urban capuchin monkeys, Sapajus sp. (Primates: cebidae). Zoologia, vol. 36, pp. 1-10. http://dx.doi.org/10.3897/zoologia.36.e30845.
http://dx.doi.org/10.3897/zoologia.36.e3...
). Some authors have even suggested that pro-social and affiliative behaviors (grooming, licking or kissing) might have been in part, evolved in the microbial transmission (Ezenwa et al., 2012EZENWA, V.O., GERARDO, N.M., INOUYE, D.W., MEDINA, M. and XAVIER, J.B., 2012. Animal behavior and the microbiome. Science, vol. 338, no. 6104, pp. 198-199. http://dx.doi.org/10.1126/science.1227412. PMid:23066064.
http://dx.doi.org/10.1126/science.122741...
). The gastrointestinal microbiota of primates is composed by a diverse microbial community, including Enterococcus sp (Lebreton et al., 2014LEBRETON, F., WILLEMS, R.J.L. and GILMORE, M.S., 2014. Enterococcus diversity, origins in nature, and gut colonization. In: M.S. GILMORE, D.B. CLEWELL, Y. IKE and N. SHANKAR, eds. Enterococci from commensals to leading causes of drug resistant infection. Boston: Massachusetts Eye and Ear Infirmary, pp. 1-52.). The idea of interaction between microbiota and behavior have stimulates the development of novel research to analyze the social contact and acquisition/exchange of commensal and symbiotic microbial. Thus, our aim was to investigate if there is a correlation between oral and fecal enterococci isolated from wild black capuchins monkeys.

Paired oral and rectal swabs were collected from five wild black capuchin monkeys living in a forest fragment in Santa Cruz do Sul - Brazil (29° 43’ 03” S; 52° 25’ 33” W). Wild capuchin monkeys were captured and manipulated using conventional methods according to the protocol for sample collection described by Instituto Chico Mendes de Conservação da Biodiversidade [ICMBio] using Tomahawk-type cages. The sample collection was approved by Information Authorization System in Biodiversity number 56640. Isolation of enterococci was performed as previously described by Santestevan et al. (2015)SANTESTEVAN, N.A., ANGELIS ZVOBODA, D., PRICHULA, J., PEREIRA, R.I., WACHHOLZ, G.R., CARDOSO, L.A., DE MOURA, T.M., MEDEIROS, A.W., AMORIN, D.B., TAVARES, M., D’AZEVEDO, P.A., FRANCO, A.C., FRAZZON, J. and FRAZZON, A.P., 2015. Antimicrobial resistance and virulence factor gene profiles of Enterococcus spp. isolates from wild Arctocephalus australis (South American fur seal) and Arctocephalus tropicalis (Subantarctic fur seal). World Journal of Microbiology & Biotechnology, vol. 31, no. 12, pp. 1935-1946. http://dx.doi.org/10.1007/s11274-015-1938-7. PMid:26347323.
http://dx.doi.org/10.1007/s11274-015-193...
. Collected bacteria were identified by MALDI-TOF MS and PCR amplification. Similarity between RAPD fingerprints was calculated using the simple association coefficient and cluster analysis, applying the Unweighted Pair Group Method with Arithmetic Mean (UPGMA). The strains grouping coefficients of similarity of ˃ 75% for RAPD typing were applied.

A total 114 Enterococcus spp. were isolated from paired samples, being E. faecalis (n=96) and E. casseliflavus (n=14) detected in both cavities, and E. hirae (n=4) only in one oral cavity. Using RAPD, we assessed the genetic relationships between oral and rectal strains, and the results showed an inter- or intra-transmission of enterococci among the monkeys. Clusters IV, V and XVII were composed by oral and rectal strains isolated from the same monkey, suggesting that autocoprophagy as mechanism of enterococci transmission. The clusters XI and XI were also formed by oral and rectal strains; however, these were isolated from different monkey suggesting that allocoprophagy as another mechanism of enterococci transmission. Two other clusters were formed by enterococci species isolated from rectal swabs from different monkey, suggesting that these bacteria might be transmitted through affiliative behavior (Figure 1). There are good evidences that gut microbial manipulate the food cravings in hosts to optimal resource for bacterial growth and induce host social interaction to facility the bacterial transmission. In addition, Schmidt et al. (2019)SCHMIDT, T.S., HAYWARD, M.R., COELHO, L.P., LI, S.S., COSTEA, P.I., VOIGT, A.Y., WIRBEL, J., MAISTRENKO, O.M., ALVES, R.J., BERGSTEN, E., DE BEAUFORT, C., SOBHANI, I., HEINTZ-BUSCHART, A., SUNAGAWA, S., ZELLER, G., WILMES, P. and BORK, P., 2019. Extensive transmission of microbes along the gastrointestinal tract. eLife, vol. 8, no. e42693, pp. 1-18. http://dx.doi.org/10.7554/eLife.42693. PMid:30747106.
http://dx.doi.org/10.7554/eLife.42693...
demonstrated the oral-fecal transmission and suggested that this transmission is an important process that shapes the gastrointestinal microbiota in health and disease.

Figure 1
Unweighted Pair Group Method with Arithmetic Mean-dendrogram showing clustering pattern for 26 genotypes of enterococci isolated from paired oral (O) and rectal (R) swabs of black capuchin monkeys (Sapajus nigritus-SN). UPGMA using Sorensen-Dice coefficients of similarity (˃ 75%).

Therefore to our knowledge, this is the first study that reports the genetic relationships between oral and rectal enterococci isolated from wild black capuchin monkeys. In conclusion, despite of the fact that a low number of samples were used for comparison- justified by the difficulties to find and capture wild monkeys- this preliminary analysis suggest that coprophagy and affiliative behaviors might have an important role in shaping and maintenance of enterococci in wild monkeys. In addition, to exploring of interactions of social dynamics and microbiota in wild populations, could be an insight for future research.

Acknowledgements

This work was performed within the framework of Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), a foundation linked to the Brazilian Ministry of Education that operates in the expansion and consolidation of stricto sensu graduate programs in all Brazilian states and sponsored by Conselho Nacional de Desenvolvimento Científico (CNPq - # 407886/2018-4, and # 302574/2017-4).

References

  • BACK, J.P., SUZIN, A. and AGUIAR, L.M., 2019. Activity budget and social behavior of urban capuchin monkeys, Sapajus sp. (Primates: cebidae). Zoologia, vol. 36, pp. 1-10. http://dx.doi.org/10.3897/zoologia.36.e30845
    » http://dx.doi.org/10.3897/zoologia.36.e30845
  • EZENWA, V.O., GERARDO, N.M., INOUYE, D.W., MEDINA, M. and XAVIER, J.B., 2012. Animal behavior and the microbiome. Science, vol. 338, no. 6104, pp. 198-199. http://dx.doi.org/10.1126/science.1227412 PMid:23066064.
    » http://dx.doi.org/10.1126/science.1227412
  • LEBRETON, F., WILLEMS, R.J.L. and GILMORE, M.S., 2014. Enterococcus diversity, origins in nature, and gut colonization. In: M.S. GILMORE, D.B. CLEWELL, Y. IKE and N. SHANKAR, eds. Enterococci from commensals to leading causes of drug resistant infection. Boston: Massachusetts Eye and Ear Infirmary, pp. 1-52.
  • SANTESTEVAN, N.A., ANGELIS ZVOBODA, D., PRICHULA, J., PEREIRA, R.I., WACHHOLZ, G.R., CARDOSO, L.A., DE MOURA, T.M., MEDEIROS, A.W., AMORIN, D.B., TAVARES, M., D’AZEVEDO, P.A., FRANCO, A.C., FRAZZON, J. and FRAZZON, A.P., 2015. Antimicrobial resistance and virulence factor gene profiles of Enterococcus spp. isolates from wild Arctocephalus australis (South American fur seal) and Arctocephalus tropicalis (Subantarctic fur seal). World Journal of Microbiology & Biotechnology, vol. 31, no. 12, pp. 1935-1946. http://dx.doi.org/10.1007/s11274-015-1938-7 PMid:26347323.
    » http://dx.doi.org/10.1007/s11274-015-1938-7
  • SCHMIDT, T.S., HAYWARD, M.R., COELHO, L.P., LI, S.S., COSTEA, P.I., VOIGT, A.Y., WIRBEL, J., MAISTRENKO, O.M., ALVES, R.J., BERGSTEN, E., DE BEAUFORT, C., SOBHANI, I., HEINTZ-BUSCHART, A., SUNAGAWA, S., ZELLER, G., WILMES, P. and BORK, P., 2019. Extensive transmission of microbes along the gastrointestinal tract. eLife, vol. 8, no. e42693, pp. 1-18. http://dx.doi.org/10.7554/eLife.42693 PMid:30747106.
    » http://dx.doi.org/10.7554/eLife.42693
  • VALENÇA-SILVA, G., MACIEL, F.G., ZAGANINI, R.L., LUCINDO, A.S., CARAMASCHI, S. and PAULA, H.M.G., 2014. Reporting social behaviours of mixed-species troops formed by Callithrix jacchus and Callithrix penicillata (Primate, Callitrichidae). Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 74, no. 3, pp. 607-611. http://dx.doi.org/10.1590/bjb.2014.0091 PMid:25296209.
    » http://dx.doi.org/10.1590/bjb.2014.0091

Publication Dates

  • Publication in this collection
    11 June 2021
  • Date of issue
    2022

History

  • Received
    01 May 2020
  • Accepted
    15 Oct 2020
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