Effects of hormonal contraception on vocal patterns of captive southern yellow-cheeked gibbons (Nomascus gabriellae)
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
40260216
PubMed Central
PMC12009915
DOI
10.3389/fvets.2025.1574926
Knihovny.cz E-zdroje
- Klíčová slova
- Nomascus, breeding programs, gibbon, vocalization, zoo,
- Publikační typ
- časopisecké články MeSH
The effects of hormonal contraception in non-human primates have been studied predominantly in relation to reproductive physiology. To date, no study has investigated how hormonal contraception affects vocal patterns in non-human primates. As part of our long-term research into the vocal behavior of southern yellow-cheeked gibbons (Nomascus gabriellae) in zoos, we have managed to obtain vocal datasets from four adult contracepted (Nexplanon® and Depo-Provera®) females of this species. In addition, we also recorded coda vocalizations (i.e., male calls added after the completion of the great call) from three paired males who are partners of three of the four females studied. We quantified 11 acoustic features in the female great calls and five acoustic features in the male coda vocalizations, for which we applied a Principal Component Analysis (PCA) and subsequently components were tested using multivariate Generalized Linear Mixed Models (GLMM). Our study revealed that hormonal contraception did indeed affect the vocal structure of great call in southern yellow-cheeked gibbon females. In contrast, our study did not reveal any flexible adjustment of the structure of the coda vocalization in direct response to changes in the females' song. In female great call, we found that the Group 1 call component and Group 2 call component were not affected by the hormonal contraceptive (Depo-Provera®) in the during-application period. However, it was noteworthy that once the effects of contraception had worn off (post-application period), the values of components did not return to pre-application periods but continued to change. Conversely, although the values of the Group 1 call component and Group 2 call component were most greatly affected by the contraceptive Nexplanon® (during-application period). The values of both components tended to return to pre-treatment levels once the effects had waned. There was a change in the values of the Group 3 call component only after application of the contraceptive Nexplanon®. These values remained significantly higher than the values at the pre-application level once the effects waned. This study provides the first evidence of changes in the stable vocal patterns of female southern yellow-cheeked gibbons as a consequence of the application of hormonal contraception.
Zobrazit více v PubMed
Asa CS. The development of contraceptive methods for captive wildlife In: Kreeger TJ, editor. Contraception in wildlife management. Washington, DC: U.S. Government Printing Office; (1997). 235–40.
Asa C, Moresco A. Fertility control in wildlife: review of current status, including novel and future technologies. Adv Exp Med Biol. (2019) 1200:507–43. doi: 10.1007/978-3-030-23633-5_17, PMID: PubMed DOI
Glatston AR. The control of zoo populations with special reference to primates. Anim Welf. (1998) 7:269–81.
Wallace PY, Asa CS, Agnew M, Cheyne SM. A review of population control methods in captive-housed primates. Anim Welf. (2016) 25:7–20. doi: 10.7120/09627286.25.1.007 DOI
Nederlof RA, Bruins-van Sonsbeek LGR, Stumpel JBG, Bakker J. Update on current hormonal and non-hormonal contraceptive options in non-human Primates. J Zool Bot Gard. (2024) 5:606–29. doi: 10.3390/jzbg5040041, PMID: PubMed DOI
Asa CS, Porton IJ, Junge R. Reproductive cycles and contraception of black lemurs (Eulemur macaco macaco) with depot medroxyprogesterone acetate during the breeding season. Zoo Biol. (2007) 26:289–98. doi: 10.1002/zoo.20136, PMID: PubMed DOI
Agnew MK, Asa CS, Clyde VL, Keller DL, Meinelt A. A survey of bonobo (Pan paniscus) oral contraceptive pill use in North American zoos. Zoo Biol. (2016) 35:444–53. doi: 10.1002/zoo.21310, PMID: PubMed DOI
Bourry O, Peignot P, Rouquet P. Contraception in the chimpanzee: 12-year experience at the CIRMF primate Centre. Gabon J Med Primatol. (2005) 34:25–34. doi: 10.1111/j.1600-0684.2004.00088.x, PMID: PubMed DOI
DeMatteo KE, Porton IJ, Asa CS. Comments from the AZA contraception advisory group on evaluating the suitability of contraceptive methods in golden-headed lion tamarins (Leontopithecus chrysomelas). Anim Welf. (2002) 11:343–8. doi: 10.1017/S0962728600024921 DOI
De Vleeschouwer K, Van Elsacker L, Heistermann M, Leus K. An evaluation of the suitability of contraceptive methods in golden-headed lion tamarins (Leontopithecus chrysomelas), with emphasis on melengestrol acetate (MGA) implants: (II) endocrinological and behavioural effects. Anim Welf. (2000) 9:385–401. doi: 10.1017/S0962728600022971, PMID: PubMed DOI
De Veeschouwer K, Leus K, Van Elsacker L. Re-assessing the reversibility of melengestrol acetate (MGA) implants in golden-headed lion tamarins (Leontopithecus chrysomelas): a comparison with golden lion tamarins (Leontopithecus rosalia). Anim Welf. (2004) 13:183–91. doi: 10.1017/S0962728600026920 DOI
Nagle CA, Lahoz MM, Porta MM, Torres M, Manzur T, Farinati Z. Suppression of ovulation by a synthetic progestin in the capuchin monkey. J Med Primatol. (2009) 38:340–6. doi: 10.1111/j.1600-0684.2009.00357.x, PMID: PubMed DOI
Wheaton CJ, Savage A, Shukla A, Neiffer D, Qu W, Sun Y, et al. . The use of long acting subcutaneous Levonorgestrel (LNG) gel depot as an effective contraceptive option for cotton-top tamarins (Saguinus oedipus). Zoo Biol. (2011) 30:498–522. doi: 10.1002/zoo.20354 PubMed DOI
Jensen JT, Hanna C, Mishler E, Lim JY, Slayden OD. Effect of menstrual cycle phase and hormonal treatments on evaluation of tubal patency in baboons. J Med Primatol. (2018) 47:40–5. doi: 10.1111/jmp.12317, PMID: PubMed DOI PMC
McDonald MM, Agnew MK, Asa CS, Powell DM. Melengestrol acetate contraceptive implant use in colobus monkeys (Colobus guereza): patterns through time and differences in reproductive potential and live births. Zoo Biol. (2020) 40:124–34. doi: 10.1002/zoo.21581, PMID: PubMed DOI
Möhle U, Heistermann M, Einspanier A, Hodges JK. Efficacy and effects of short- and medium-term contraception in the common marmoset (Callithrix jacchus) using melengestrol acetate implants. J Med Primatol. (1999) 28:36–47. doi: 10.1111/j.1600-0684.1999.tb00087.x, PMID: PubMed DOI
Crawford JC, Boulet M, Drea CM. Smelling wrong: hormonal contraception in lemurs alters critical female odour cues. Proc R Soc Lond B Biol Sci. (2011) 278:122–30. doi: 10.1098/rspb.2010.1203, PMID: PubMed DOI PMC
Guy AJ, Schuerch F, Heffernan S, Thomson PC, O'Brien JK, McGreevy PD. The effect of medroxyprogesterone acetate on behavioural responses of captive female hamadryas baboons (Papio hamadryas). Ani Repro Sci. (2008) 108:412–24. doi: 10.1016/j.anireprosci.2007.09.008, PMID: PubMed DOI
Maijer AM, Semple S. Investigating potential effects of the contraceptive Implanon on the behavior of free-ranging adult female barbary macaques. J Appl Anim Welf Sci. (2016) 19:16–23. doi: 10.1080/10888705.2015.1083432, PMID: PubMed DOI
Steklis HD, Linn GS, Howard SM, Kling AS, Tiger L. Effects of medroxyprogesterone acetate on socio-sexual behaviour of stumptail macaques. Physiol Behav. (1982) 28:535–44. doi: 10.1016/0031-9384(82)90152-4, PMID: PubMed DOI
Karaskiewicz CL, Ramirez M, Bales KL. Physiological and behavioral effects of hormonal contraceptive treatment in captive, pair-bonded primates (Plecturocebus cupreus). J Am Assoc Lab Anim Sci. (2023) 62:494–501. doi: 10.30802/AALAS-JAALAS-23-000017, PMID: PubMed DOI PMC
Amir O, Kishon-Rabin L. Association between birth control pills and voice quality. Laryngoscope. (2004) 114:1021–6. doi: 10.1097/00005537-200406000-00012, PMID: PubMed DOI
Banai IP. Voice in different phases of menstrual cycle among naturally cycling women and users of hormonal contraceptives. PLoS One. (2017) 12:e0183462. doi: 10.1371/journal.pone.0183462, PMID: PubMed DOI PMC
Morris RJ, Gorham-Rowan MM, Harmon AB. The effect of initiating Oral contraceptive use on voice: a case study. J Voice. (2011) 25:223–9. doi: 10.1016/j.jvoice.2009.08.006, PMID: PubMed DOI
Geissmann T. Duet-splitting and the evolution of gibbon songs. Biol Rev. (2002) 77:57–76. doi: 10.1017/s1464793101005826, PMID: PubMed DOI
Haimoff E. Acoustic and organizational features of gibbon song In: Preuschoft H, Chivers DJ, Brockelman WY, Creel N, editors. The lesser apes: Evolutionary and behavioural biology. Edinburgh University: Edinburgh Press; (1984). 390–403.
Konrad R, Geissmann T. Vocal diversity and taxonomy of Nomascus in Cambodia. Int J Primatol. (2006) 27:713–45. doi: 10.1007/s10764-006-9042-3 DOI
Terleph TA, Malaivijitnond S, Reichard UH. Age related decline in female Lar gibbon great call performance suggests that call features correlate with physical condition. BMC Evol Biol. (2016) 16:4. doi: 10.1186/s12862-015-0578-8, PMID: PubMed DOI PMC
Hradec M, Illmann G, Prikrylová M. Bolechová P and Vostrá-Vydrová H difference in the songs of paired and unpaired southern yellow-cheeked gibbon males (Nomascus gabriellae): social status or age? Front Ecol Evol. (2023) 11:956922. doi: 10.3389/fevo.2023.956922 DOI
Terleph TA, Malaivijitnond S, Reichard UH. An analysis of white-handed gibbon male song reveals speech-like phrases. Am J Phys Anthropol. (2018) 166:649–60. doi: 10.1002/ajpa.23451, PMID: PubMed DOI
Lefaux B, Ford M, Dobbs T, Souvignet T, Stumpel J, Bugg L, et al. . Long-term management plan for the Gibbon EAZA ex situ Programmes (EEPs). European Association of Zoos and Aquaria (EAZA) pp. 1–42. (2020).
Asa CS, Porton IJ. Wildlife contraception: Issues, methods and applications. Baltimore, MD: John Hopkins University Press; (2005). 288 p.
R Core Team . R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; (2024).
Lenth RV. Least-squares means: the R Packa gels means. J Stat Soft. (2016) 69:1–33. doi: 10.18637/jss.v069.i01 DOI
Maaskant A, Scarsi KK, Meijer L, Roubos S, Louwerse AL, Remarque EJ, et al. . Long-acting reversible contraception with etonogestrel implants in female macaques (Macaca mulatta and Macaca fascicularis). Front Vet Sci. (2024) 10:1319862. doi: 10.3389/fvets.2023.1319862, PMID: PubMed DOI PMC
Hradec M, Illmann G, Bartoš L, Bolechová P. The transition from the female-like great calls to male calls during ontogeny in southern yellow-cheeked gibbon males (Nomascus gabriellae). Sci Rep. (2021) 11:22040. doi: 10.1038/s41598-021-01648-x, PMID: PubMed DOI PMC
Species360 . Zoological Information Management System (ZIMS). (2024). Available online at: https://zims.Species360.org.
Brockelman WY, Schilling D. Inheritance of stereotyped gibbon calls. Nature. (1984) 312:634–6. doi: 10.1038/312634a0, PMID: PubMed DOI
Cowlishaw G. Song function in gibbons. Behaviour. (1992) 121:131–53. doi: 10.1163/156853992X00471 DOI
Geissmann T, Orgeldinger M. The relationship between duet songs and pair bonds in siamangs, Hylobates syndactylus. Anim Behav. (2000) 60:805–9. doi: 10.1006/anbe.2000.1540, PMID: PubMed DOI
Linn GS, Steklis HD. The effects of depo-medroxyprogesterone acetate (DMPA) on copulation-related and agonistic behaviors in an island colony of stumptail macaques (Macaca arctoides). Physiol Behav. (1990) 47:403–8. doi: 10.1016/0031-9384(90)90100-i, PMID: PubMed DOI
Taberer TR, Mead J, Hartley M, Harvey ND. Impact of female contraception for population management on behavior and social interactions in a captive troop of Guinea baboons (Papio papio). Zoo Biol. (2023) 42:254–67. doi: 10.1002/zoo.21728, PMID: PubMed DOI
Portugal MM, Asa CS. Effects of chronic melengestrol acetate contraceptive treatment on perineal tumescence, body weight, and sociosexual behavior of hamadryas baboons (Papio hamadryas). Zoo Biol. (1995) 14:251–9. doi: 10.1002/zoo.1430140306, PMID: PubMed DOI
Reichard UH. “Social monogamy in gibbons: the male perspective”. In: Reichard UH, and Boesch C, editors. Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge: Cambridge University Press. (2003) p 190–213.