The environment matters: season and female contact affect the behavior of captive Addax nasomaculatus male antelope

Akaike H (1974) A new look at the statistical model identification. IEEE Trans. Automat. Contr 19:716–723. https://doi.org/10.1109/TAC.1974.1100705 Alvarez F (1993) Risks of fighting in relation to age and territory holding in fallow deer. Can J Zool 71:376–383. https://doi.org/10.1139/z93-052 Apollonio M, Di Vittorio I (2004) Feeding and reproductive behaviour in fallow bucks (Dama dama). Naturwissenschaften 91:579–584. https://doi.org/10.1007/s00114-004-0574-0 Brashares JS, Arcese P (1999) Scent marking in a territorial African antelope: II. The economics of marking with faeces. Anim Behav 57:11–17. https://doi.org/10.1006/anbe.1998.0942 Bronson FH (1989) Mammalian reproductive biology. The University of Chicago Press, Chicago Brivio F, Grignolio S, Apollonio M (2010) To feed or not to feed? Testing different hypotheses on rut-induced hypophagia in a mountain ungulate. Ethology 116:406–415. https://doi.org/10.1111/j.1439-0310.2010.01753.x Carrillo E, Tejada LM, Meza-Herrera CA, Arellano-Rodríguez G, García JE, De Santiago Miramontes MA, Mellado M, Véliz FG (2011) Response of sexual inactive French Alpine bucks to the stimulus of goats in oestrus. Livest Sci 141:202–206. https://doi.org/10.1016/j.livsci.2011.06.004 Clausen N, Houston B, Their T, Enright W, Spevak E, Fisher M (2014) Addax (Addax nasomaculatus) AZA animal program population viability analysis report. Association of Zoos and Aquariums (AZA). Available in: https://ams.aza.org/iweb/upload/Population%20Viability%20Analysis%20(PVA)%20Report%20-%202014%20Addax%20AZA%20Animal%20Program-58a15fec.pdf. Accessed 07 Feb 2023 Clutton-Brock T, Guinness FE, Albon SD (1982) Red beer: behavior and ecology of two sexes. University of Chicago, Chicago Clutton-Brock TH, Huchard E (2013) Social competition and selection in males and females. Phil Trans R Soc B 368:20130074. https://doi.org/10.1098/rstb.2013.0074 Corlatti L, Bassano B (2014) Contrasting alternative hypotheses to explain rut-induced hypophagia in territorial male chamois. Ethology 120:32–41. https://doi.org/10.1111/eth.12177 Densmore MA, Kraemer DC (1986) Analysis of reproductive data on the addax: in captivity. Int Zoo Yearb 24:303–306. https://doi.org/10.1111/j.1748-1090.1985.tb02559.x Dicks KL, Bal AD, Banfield L, Barrios V, Boufaroua M, Chetoui A, Chuven J, Craig M, Al Faqeer MY, Mallam Garba HH, Guedara H, Harouna A, Ivy J, Najjar C, Petretto M, Pusey R, Rabeil T, Riordan P, Senn HV, Taghouti E, Wacher T, Tim W, Gilbert T (2022) Genetic diversity in global populations of the critically endangered addax (Addax nasomaculatus) and its implications for conservation. Evol Appl 16:111–125. https://doi.org/10.1111/eva.13515 Dittrich L (1972) Gestation periods and age of sexual maturity of some African antelopes. Int Zoo Yearb 12:184–187. https://doi.org/10.1111/j.1748-1090.1972.tb02322.x Giriboni J, Lacuesta L, Ungerfeld R (2017) Continuous contact with females in estrus throughout the year enhances testicular activity and improves seminal traits of male goats. Theriogenology 87:284–289. https://doi.org/10.1016/j.theriogenology.2016.09.004 Goncalvez-Maia G, Bruno-Siqueira LG, de Paula-Vasconcelos CO, Ribeiro-Tomich T, de Almeida-Camargo LS, Pacheco-Rodrigues JP, Araujo-de Menezes R, Goncalvez LC, Faggion-Teixeira B, de Olivera-Grando R, Garcia-Nogueira LA, Ribeiro-Pereira LG (2020) Effects of heat stress on rumination activity in Holstein-Gyr dry cows. Livest Sci 239:104092. https://doi.org/10.1016/j.livsci.2020.104092 Gonzalez R, Orgeur P, Signoret JP (1988a) Luteinizing hormone, testosterone and cortisol responses in rams upon presentation of estrous females in the nonbreeding season. Theriogenology 30:1075–1086. https://doi.org/10.1016/0093-691X(88)90282-8 Gonzalez R, Poindron P, Signoret JP (1988b) Temporal variation in LH and testosterone responses of rams after the introduction of oestrous females during the breeding season. Reproduction 83:201–208. https://doi.org/10.1530/jrf.0.0830201 Gonzalez R, Orgeur P, Poindron P, Signoret JP (1991) Female effect in sheep I. The effects of sexual receptivity of females and the sexual experience of rams. Reprod Nutr Dev 31:97–102 Gosling LM, Roberts SC (2001) Scent-marking by male mammals: cheat-proof signals to competitors and mates. Adv Study Behav 30:169–217. https://doi.org/10.1016/S0065-3454(01)80007-3 Grubb P (1974) Population dynamics of the Soay sheep. In: Jewell PA, Milner C, Morton Boyd J (eds) Island Survivors; the ecology of the Soay Sheep of St. Kilda, Athlone Press, London, pp 242–272 Hizem MW, Riordan P, El-Farhati H, Hamdi L, Nouira S (2019) Temporal patterns in natality and mortality of three threatened antelope species in North Africa: Oryx dammah, Addax nasomaculatus and Nanger dama. Afr J Ecol 57:575–585. https://doi.org/10.1111/aje.12606 Hirayama T, Oshiro S, Katoh K, Ohta M (2000) Effects of heat exposure on the rumination and passage rate of feeds through the digestive tract of goats. Anim Sci J 71:258–263 Hummel J, Steuer P, Südekum KH, Hammer S, Hammer C, Streich WJ, Clauss M (2008) Fluid and particle retention in the digestive tract of the addax antelope (Addax nasomaculatus)—adaptations of a grazing desert ruminant. Comp Biochem Physiol Part A Mol Integr Physiol 149:142–149. https://doi.org/10.1016/j.cbpa.2007.11.001 Hart BL (1974) Gonadal androgen and socio-sexual behavior of male mammals: a comparative analysis. Psych Bull 81:383–400 Illius AW, Haynes NB, Lamming GE (1976) Effects of ewe proximity on peripheral plasma testosterone levels and behaviour in the ram. J Reprod Infertil 48:25–32. https://doi.org/10.1530/jrf.0.0480025 International Studbooks for Rare Species of Wild Animals in Captivity (2018) Int Zoo Yearb 52:448–478. https://doi.org/10.1111/izy.12194. IUCN (2023) The IUCN red list of threatened species 2016. Available in: https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T512A50180603. Accessed 07 Feb 2023 Katongole CB, Naftolin F, Short RV (1971) Relationship between blood levels of luteinizing hormone and testosterone in bulls, and the effects of sexual stimulation. J Endocrinol 50:457–466. https://doi.org/10.1677/joe.0.0500457 Krausman PR, Casey AL (2007) Addax Nasomaculatus Mamm Species 2007:1–4. https://doi.org/10.1644/807.1 Kamgang VW, Bennett NC, Hart DW, Van der Goot AC, Ganswindt A (2020) Reproductive events and respective faecal androgen metabolite concentrations in captive male roan antelope (Hippotragus equinus). Plos one 15:e0243277. https://doi.org/10.1371/journal.pone.0243277. Lincoln GA, Guinness F, Short RV (1972) The way in which testosterone controls the social and sexual behavior of the red deer stag (Cervus elaphus). Horm Behav 3:375–396. https://doi.org/10.1016/0018-506X(72)90027-X Lincoln GA (2001) The irritable male syndrome. Reprod Fertil Dev 13:567–576. https://doi.org/10.1071/RD01077 Llonch L, Castillejos L, Ferret A (2020) Increasing the content of physically effective fiber in high-concentrate diets fed to beef heifers affects intake, sorting behavior, time spent ruminating, and rumen pH. J Anim Sci 98:1–9. https://doi.org/10.1093/jas/skaa192 Longpre KM, Guterl JN, Katz LS (2016) Proximity to females alters circulating testosterone concentrations and body weight in male goats. Small Rum Res 144:334–340. https://doi.org/10.1016/j.smallrumres.2016.10.014 Malfatti A, Barbato O, Todini L, Terzano GM, Debenedetti A, Borghese A (2006) Blood testosterone levels in Italian Mediterranean buffalo bulls managed in two different breedingconditions. Theriogenology 65:1137–1144. https://doi.org/10.1016/j.theriogenology.2005.07.012 Manski DA (1991) Reproductive behavior of addax antelope. Appl Anim Behav Sci 29:39–66. https://doi.org/10.1016/0168-1591(91)90237-R Martin P, Bateson P (2007) Measuring behavior. Cambridge University Press, New York Mattiangeli V, Mattiello S, Verga M (1998) Factors affecting the duration of fights in fallow deer (Dama dama) during the rut. Ethol Ecol Evol 10:87–93. https://doi.org/10.1080/08927014.1998.9522874 Monfort SL, Brown JL, Bush M, Wood TC, Wemmer C, Vargas A, Williamson LR, Montali RJ, Wildt DE (1993) Circannual inter-relationships among reproductive hormones, gross morphometry, behaviour, ejaculate characteristics and testicular histology in Eld’s deer stags (Cervus eldi thamin). J Reprod Fert 98:471–480. https://doi.org/10.1530/jrf.0.0980471 Newman RE, McConnell SJ, Weston RH, Reeves M, Bernasconi C, Baker PJ, Wynn PC (1998) The relationship between plasma testosterone concentrations and the seasonal variation in voluntary feed intake in fallow bucks (Dama dama). J Agric Sci 130:357–366. https://doi.org/10.1017/S0021859698005279 Pelletier F, Bauman J, Festa-Bianchet M (2003) Fecal testosterone in bighorn sheep (Ovis canadensis): behavioural and endocrine correlates. Can J Zool 81:1678–1684. https://doi.org/10.1139/z03-156 Pelletier F, Mainguy J, Côté SD (2009) Rut-induced hypophagia in male bighorn sheep and mountain goats: foraging under time budget constraints. Ethology 115:141–151. https://doi.org/10.1111/j.1439-0310.2008.01589.x Ralls K (1971) Mammalian scent marking: mammals mark when dominant to and intolerant of others, not just when they possess a territory. Science 171:443–449. https://doi.org/10.1126/science.171.3970.443 Seri H, Chammem M, Ferreira LM, Kechnebou M, Khorchani T, Silva SR (2018) Effects of seasonal variation, group size and sex on the activity budget and diet composition of the addax antelope. Afr J Range Forage Sci 35:89–100. https://doi.org/10.2989/10220119.2018.1477831 Spevak EM (2015) Behavioral and genetic correlates of reproductive success in male addax (Addax nasomaculatus, De Blainville 1816). Doctoral Thesis, University of Illinois. Stabach JA, Rabeil T, Turmine V, Wacher T, Mueller T, Leimgruber P (2017) On the brink of extinction—habitat selection of addax and dorcas gazelle across the Tin Toumma desert. Niger Divers Distrib 23:581–591. https://doi.org/10.1111/ddi.12563 Sutherland JN, Becker SE, Katz LS (2022) Effect of proximity to females on integument damage caused by self-enurination in male goats. Res Vet Sci 143:1–3. https://doi.org/10.1016/j.rvsc.2021.12.007 Ungerfeld R, Giriboni J, Freitas-de-Melo A, Lacuesta L (2014) Homosexual behavior in male goats is more frequent during breeding season and in bucks isolated from females. Horm Behav 65:516–520. https://doi.org/10.1016/j.yhbeh.2014.04.013 Villagrán M, Ungerfeld R (2013) Permanent contact with females increases testosterone and improves fresh semen traits in pampas deer (Ozotoceros bezoarticus) males. Anim Reprod Sci 143:85–90. https://doi.org/10.1016/j.anireprosci.2013.10.011 Walkden- Brown SW, Restall BJ, Norton BW, Scaramuzzi RJ (1994) The “female effect” in Australian cashemere goats: effect of season and quality of diet on the LH and testosterone response of bucks to oestrous does. J Reprod Fertil 100:521–531. https://doi.org/10.1530/jrf.0.1000521 Williams CM, Henry HAL, Sinclair BJ (2015) Cold truths: how winter drives responses of terrestrial organisms to climate change. Biol Rev 90:214–235. https://doi.org/10.1111/brv.12105 Yahr P, Newman A, Stephen DR (1979) Sexual behavior and scent marking in male gerbils: comparison of changes after castration and testosterone replacement. Horm Behav 13:175–184. https://doi.org/10.1016/0018-506X(79)90056-4