Social rank does not affect sperm quality in male African wild dogs (Lycaon pictus)
Femke Van den Berghe
A B , Monique C. J. Paris B C , Zoltan Sarnyai D , Michael B. Briggs E , Robert P. Millar B F , Andre Ganswindt G H and Damien B. B. P. Paris A I J
+ Author Affiliations
- Author Affiliations
A Gamete and Embryology (GAME) Laboratory, College of Public Health, Medical and Veterinary Sciences, James Cook University, James Cook Drive, Townsville, Qld 4811, Australia.
B Institute for Breeding Rare and Endangered African Mammals (IBREAM), 9 Ainslie Place, Edinburgh, EH3 6AT, Scotland.
C Wageningen Livestock Research, De Elst 1, 6708 WD Wageningen, Netherlands.
D Laboratory of Psychiatric Neuroscience, Australian Institute of Tropical Health and Medicine (AITHM) and College of Public Health, Medical and Veterinary Sciences, James Cook University, Solander Drive, Townsville, Qld 4811, Australia.
E African Predator Conservation Research Organisation (APCRO), 848 Rainbow Boulevard #A3, Las Vegas, NV 89107, USA.
F Centre for Neuroendocrinology, Faculty of Health Sciences, University of Pretoria, Pretoria 0002, South Africa.
G Mammal Research Institute, Faculty of Natural and Agricultural Sciences, University of Pretoria, Hatfield 0028, South Africa.
H Endocrine Research Laboratory, Faculty of Veterinary Science, University of Pretoria, Onderstepoort 0110, South Africa.
I Centre for Tropical Environmental and Sustainability Science, James Cook University, James Cook Drive, Townsville, Qld 4811, Australia.
J Corresponding author. Email: damien.paris@jcu.edu.au
Reproduction, Fertility and Development 31(5) 875-887 https://doi.org/10.1071/RD18205
Submitted: 5 June 2018 Accepted: 3 December 2018 Published: 30 January 2019
Abstract
Sperm banking and AI could benefit endangered African wild dog conservation. However, it is unclear whether their dominance hierarchy causes a decrease in reproductive and sperm quality parameters in subordinate males that typically do not breed. In this study, we investigated the effect of social rank on male reproductive parameters, including faecal androgen and glucocorticoid metabolite concentrations, prostate and testes volume, preputial gland size, semen collection success and sperm quality. Samples were obtained from captive males (prebreeding season: n = 12 from four packs; breeding season: n = 24 from seven packs) that were classified as alpha (dominant), beta or gamma (subordinates) based on the frequency of dominant versus submissive behaviours. In the prebreeding season, semen was successfully collected from all alpha but only half the subordinate males, with urine contamination (associated with lower rank) significantly reducing total and progressive motility, sperm motility index, normal sperm morphology and acrosome integrity. The breeding season was associated with a significant increase in faecal androgens, prostate and testis volume, as well as progressive motility and the total number of spermatozoa ejaculated. However, with the exception of prostate volume (mean ± s.e.m: 12.5 ± 4.5, 7.1 ± 1.0 and 7.3 ± 1.0 cm3 in alpha, beta and gamma males respectively; P = 0.035), all other reproductive and sperm quality parameters did not differ between males of each social rank. In conclusion, reproductive suppression of subordinate males appears to be behaviourally mediated, because males of all social ranks produce semen of similar quality, making them suitable candidates for sperm banking, particularly during the breeding season when sperm quality improves.
Additional keywords : behaviour, cortisol, dominance, fertility, prostate, semen, testis, testosterone.
References
Asa, C. S., Bauman, K. L., Devery, S., Zordan, M., Camilo, G. R., Boutelle, S., and Moresco, A. (2014). Factors associated with uterine endometrial hyperplasia and pyometra in wild canids: implications for fertility. Zoo Biol. 33, 8–19.| Factors associated with uterine endometrial hyperplasia and pyometra in wild canids: implications for fertility.Crossref | GoogleScholarGoogle Scholar | 23553688PubMed |
Barja, I., Silvan, G., and Illera, J. C. (2008). Relationships between sex and stress hormone levels in feces and marking behavior in a wild population of Iberian wolves (Canis lupus signatus). J. Chem. Ecol. 34, 697–701.
| Relationships between sex and stress hormone levels in feces and marking behavior in a wild population of Iberian wolves (Canis lupus signatus).Crossref | GoogleScholarGoogle Scholar | 18392658PubMed |
Blanco, J. M., Gee, G. F., Wildt, D. E., and Donoghue, A. M. (2002). Producing progeny from endangered birds of prey: treatment of urine-contaminated semen and a novel intramagnal insemination approach. J. Zoo Wildl. Med. 33, 1–7.
| Producing progeny from endangered birds of prey: treatment of urine-contaminated semen and a novel intramagnal insemination approach.Crossref | GoogleScholarGoogle Scholar | 12216788PubMed |
Chen, D., Scobey, M. J., and Jeyendran, R. S. (1995). Effects of urine on the functional quality of human spermatozoa. Fertil. Steril. 64, 1216–1217.
| Effects of urine on the functional quality of human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 7589682PubMed |
Christensen, B. W., Asa, C. S., Wang, C., Vansandt, L., Bauman, K., Callahan, M., Jens, J. K., and Ellinwood, N. M. (2011). Effect of semen collection method on sperm motility of gray wolves (Canis lupus) and domestic dogs (C. l. familiaris). Theriogenology 76, 975–980.
| Effect of semen collection method on sperm motility of gray wolves (Canis lupus) and domestic dogs (C. l. familiaris).Crossref | GoogleScholarGoogle Scholar | 21752444PubMed |
Creel, S. (2001). Social dominance and stress hormones. Trends Ecol. Evol. 16, 491–497.
| Social dominance and stress hormones.Crossref | GoogleScholarGoogle Scholar |
Creel, S. F. (2005). Dominance, aggression, and glucocorticoid levels in social carnivores. J. Mammal. 86, 255–264.
| Dominance, aggression, and glucocorticoid levels in social carnivores.Crossref | GoogleScholarGoogle Scholar |
Creel, S., and Creel, N. M. (Eds) (2002). ‘The African Wild Dog. Behavior, Ecology, and Conservation.’ (University Press: Princeton.)
Creel, S., Creel, N. M., Mills, M. G. L., and Monfort, S. L. (1997). Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates. Behav. Ecol. 8, 298–306.
| Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates.Crossref | GoogleScholarGoogle Scholar |
de Villiers, M. S., van Jaarsveld, A. S., Meltzer, D. G. A., and Richardson, P. R. K. (1997). Social dynamics and the cortisol response to immobilization stress of the African wild dog, Lycaon pictus. Horm. Behav. 31, 3–14.
| Social dynamics and the cortisol response to immobilization stress of the African wild dog, Lycaon pictus.Crossref | GoogleScholarGoogle Scholar | 9109594PubMed |
Frantzen, M. A. J., Ferguson, J. W. H., and de Villiers, M. S. (2001). The conservation role of captive African wild dogs (Lycaon pictus). Biol. Conserv. 100, 253–260.
| The conservation role of captive African wild dogs (Lycaon pictus).Crossref | GoogleScholarGoogle Scholar |
Girman, D. J., Mills, M. G. L., Geffen, E., and Wayne, R. K. (1997). A molecular genetic analysis of social structure, dispersal, and interpack relationships of the African wild dog (Lycaon pictus). Behav. Ecol. Sociobiol. 40, 187–198.
| A molecular genetic analysis of social structure, dispersal, and interpack relationships of the African wild dog (Lycaon pictus).Crossref | GoogleScholarGoogle Scholar |
Gomendio, M., Malo, A. F., Garde, J., and Roldan, E. R. (2007). Sperm traits and male fertility in natural populations. Reproduction 134, 19–29.
| Sperm traits and male fertility in natural populations.Crossref | GoogleScholarGoogle Scholar | 17641085PubMed |
Johnston, S. D., Kustritz, M. V. R., and Olson, P. N. S. (2001). Semen collection, evaluation and preservation. In ‘Canine and Feline Theriogenology’. (Eds R. Kersey and D. LeMelledo.) pp. 287–306. (W. B. Saunders: Philadelphia.)
Johnston, S. D., Ward, D., Lemon, J., Gunn, I., MacCallum, C. A., Keeley, T., and Blyde, D. (2007). Studies of male reproduction in captive African wild dogs (Lycaon pictus). Anim. Reprod. Sci. 100, 338–355.
| Studies of male reproduction in captive African wild dogs (Lycaon pictus).Crossref | GoogleScholarGoogle Scholar | 16987622PubMed |
Kim, S. C., and Kim, H. W. (1998). Effects of nitrogenous components of urine on sperm motility: an in vitro study. Int. J. Androl. 21, 29–33.
| Effects of nitrogenous components of urine on sperm motility: an in vitro study.Crossref | GoogleScholarGoogle Scholar | 9639149PubMed |
Lewis, S. E., and Aitken, R. J. (2005). DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res. 322, 33–41.
| DNA damage to spermatozoa has impacts on fertilization and pregnancy.Crossref | GoogleScholarGoogle Scholar | 15912407PubMed |
Monfort, S. L., Wasser, S. K., Mashburn, K. L., Burke, M., Brewer, B. A., and Creel, S. R. (1997). Steroid metabolism and validation of noninvasive endocrine monitoring in the African wild dog (Lycaon pictus). Zoo Biol. 16, 533–548.
| Steroid metabolism and validation of noninvasive endocrine monitoring in the African wild dog (Lycaon pictus).Crossref | GoogleScholarGoogle Scholar |
Mouiex, C. (2006). Genetic verification of multiple paternity in two free-ranging isolated populations of African wild dogs (Lycaon pictus). M.Sc. Thesis, University of Pretoria.
Newell-Fugate, A. E., Nothling, J. O., and Bertschinger, H. J. (2012). Seasonal changes in steroid hormone profiles, body weight, semen quality, and the reproductive tract in captive African wild dogs (Lycaon pictus) in South Africa. Gen. Comp. Endocrinol. 178, 272–281.
| Seasonal changes in steroid hormone profiles, body weight, semen quality, and the reproductive tract in captive African wild dogs (Lycaon pictus) in South Africa.Crossref | GoogleScholarGoogle Scholar | 22683282PubMed |
O’Brien, J. K., Steinman, K. J., Montano, G. A., Love, C. C., and Robeck, T. R. (2013). Sperm DNA fragmentation and morphological degeneration in chilled elephant (Elephas maximus and Loxodonta Africana) semen collected by transrectal massage. Andrology 1, 387–400.
| Sperm DNA fragmentation and morphological degeneration in chilled elephant (Elephas maximus and Loxodonta Africana) semen collected by transrectal massage.Crossref | GoogleScholarGoogle Scholar | 23536498PubMed |
Ohl, D. A., Denil, J., Cummins, C., Menge, A. C., and Seager, S. W. J. (1994). Electroejaculation does not impair sperm motility in the beagle dog: a comparative study of electroejaculation and collection by artificial vagina. J. Urol. 152, 1034–1037.
| Electroejaculation does not impair sperm motility in the beagle dog: a comparative study of electroejaculation and collection by artificial vagina.Crossref | GoogleScholarGoogle Scholar | 8051729PubMed |
Palme, R., and Mostl, E. (1994). Biotin–streptavidin enzyme immunoassay for the determination of oestrogen and androgens in boar faeces. In ‘Advances of Steroid Analysis ’93’. (Ed. E. S. Görög.) pp. 111–117. (Akadémiai Kiadó: Budapest.)
Palme, R., and Mostl, E. (1997). Measurement of cortisol metabolites in faeces of sheep as a parameter of cortisol concentration in blood. Mamm. Biol. 62, 192–197.
Paris, D. B., Taggart, D. A., Shaw, G., Temple-Smith, P. D., and Renfree, M. B. (2005). Changes in semen quality and morphology of the reproductive tract of the male tammar wallaby parallel seasonal breeding activity in the female. Reproduction 130, 367–378.
| Changes in semen quality and morphology of the reproductive tract of the male tammar wallaby parallel seasonal breeding activity in the female.Crossref | GoogleScholarGoogle Scholar | 16123244PubMed |
Preston, B. T., Stevenson, I. R., Pemberton, J. M., and Wilson, K. (2001). Dominant rams lose out by sperm depletion – a waning success in siring counters a ram’s high score in competition for ewes. Nature 409, 681–682.
| Dominant rams lose out by sperm depletion – a waning success in siring counters a ram’s high score in competition for ewes.Crossref | GoogleScholarGoogle Scholar | 11217847PubMed |
Ren, L., Li, X., Weng, Q., Trisomboon, H., Yamamoto, T., Pan, L., Watanabe, G., and Taya, K. (2010). Effects of acute restraint stress on sperm motility and secretion of pituitary, adrenocortical and gonadal hormones in adult male rats. J. Vet. Med. Sci. 72, 1501–1506.
| Effects of acute restraint stress on sperm motility and secretion of pituitary, adrenocortical and gonadal hormones in adult male rats.Crossref | GoogleScholarGoogle Scholar | 20606370PubMed |
Restelli, A. E., Bertolla, R. P., Spaine, D. M., Miotto, A., Borrelli, M., and Cedenho, A. P. (2009). Quality and functional aspects of sperm retrieved through assisted ejaculation in men with spinal cord injury. Fertil. Steril. 91, 819–825.
| Quality and functional aspects of sperm retrieved through assisted ejaculation in men with spinal cord injury.Crossref | GoogleScholarGoogle Scholar | 18353315PubMed |
Ruel, Y., Barthez, P. Y., Mailles, A., and Begon, D. (1998). Ultrasonographic evaluation of the prostate in healthy intact dogs. Vet. Radiol. Ultrasound 39, 212–216.
| Ultrasonographic evaluation of the prostate in healthy intact dogs.Crossref | GoogleScholarGoogle Scholar | 9634189PubMed |
Santos, I., Cunha, I., and Melo, E. (2011). Effects of urine and NaCl solutions of different osmolarities on canine sperm. Anim. Reprod. Sci. 8, 73–76.
Sasagawa, I., Yazawa, H., Suzuki, Y., and Nakada, T. (2001). Stress and testicular germ cell apoptosis. Arch. Androl. 47, 211–216.
| Stress and testicular germ cell apoptosis.Crossref | GoogleScholarGoogle Scholar | 11695845PubMed |
Seli, E., Gardner, D. K., Schoolcraft, W. B., Moffatt, O., and Sakkas, D. (2004). Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization. Fertil. Steril. 82, 378–383.
| Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 15302287PubMed |
Spiering, P. A., Somers, M. J., Maldonado, J. E., Wildt, D. E., and Gunther, M. S. (2010). Reproductive sharing and proximate factors mediating cooperative breeding in the African wild dog (Lycaon pictus). Behav. Ecol. Sociobiol. 64, 583–592.
| Reproductive sharing and proximate factors mediating cooperative breeding in the African wild dog (Lycaon pictus).Crossref | GoogleScholarGoogle Scholar |
Van den Berghe, F., Paris, D. B., Van Soom, A., Rijsselaere, T., Van der Weyde, L., Bertschinger, H. J., and Paris, M. C. (2012). Reproduction in the endangered African wild dog: basic physiology, reproductive suppression and possible benefits of artificial insemination. Anim. Reprod. Sci. 133, 1–9.
| Reproduction in the endangered African wild dog: basic physiology, reproductive suppression and possible benefits of artificial insemination.Crossref | GoogleScholarGoogle Scholar | 22748701PubMed |
Van den Berghe, F., Paris, M. C. J., Briggs, M. B., Farstad, W. K., and Paris, D. B. B. P. (2018a). A two-step dilution Tris-egg yolk extender containing Equex STM significantly improves sperm cryopreservation in the African wild dog (Lycaon pictus). Cryobiology 80, 18–25.
| A two-step dilution Tris-egg yolk extender containing Equex STM significantly improves sperm cryopreservation in the African wild dog (Lycaon pictus).Crossref | GoogleScholarGoogle Scholar | 29287895PubMed |
Van den Berghe, F., Paris, M. C. J., Sarnyai, Z., Vlamings, B., Millar, R. P., Ganswindt, A., Cozzi, A., Pageat, P., and Paris, D. B. B. P. (2018b). Dog appeasing pheromone prevents the androgen surge and may reduce contact dominance and active submission after stressful interventions in African wild dogs (Lycaon pictus). PLoS One , .
Van der Weyde, L. K. (2013). Reproductive biology of the endangered African wild dog (Lycaon pictus) in captive and free-ranging populations: an endocrine, behavioural and demographic approach. Ph.D. Thesis, University of Western Australia, Perth.
Van der Weyde, L. K., Martin, G. B., Blackberry, M. A., Gruen, V., Harland, A., and Paris, M. C. (2015). Reproductive hormonal patterns in pregnant, pseudopregnant and acyclic captive African wild dogs (Lycaon pictus). Anim. Reprod. Sci. 156, 75–82.
| Reproductive hormonal patterns in pregnant, pseudopregnant and acyclic captive African wild dogs (Lycaon pictus).Crossref | GoogleScholarGoogle Scholar | 25818522PubMed |
Van Heerden, J., and Kuhn, F. (1985). Reproduction in captive hunting dogs Lycaon pictus. S. Afr. J. Wildl. Res. 15, 80–84.
Vlamings, B. H. A. C. (2011). Dog appeasing pheromone®: A useful tool to minimize stress and aggression of African wild dogs (Lycaon pictus)? MSc Thesis, University of Utrecht, Utrecht, the Netherlands.
Woodroffe, R., and Sillero-Zubiri, C. (2012). Lycaon pictus. The IUCN Red List of Threatened Species, Version 2017–1. Available at http://dx.doi.org/10.2305/IUCN.UK.2012.RLTS.T12436A16711116.en [verified 12 July 2017].
Young, A. J., Carlson, A. A., Monfort, S. L., Russell, A. F., Bennett, N. C., and Clutton-Brock, T. (2006). Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc. Natl Acad. Sci. USA 103, 12005–12010.
| Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats.Crossref | GoogleScholarGoogle Scholar | 16894179PubMed |
