Unintended consequences of contraception management
Contraception and group fidelity
Feral horse populations have expanded across the United Sates, making them the subject of considerable controversy. The extirpation of their natural predators and land use conflicts with humans all but necessitate some form of population management wherever feral horses occur. Given the options, contraception appears the most humane, providing population control, while avoiding more invasive measures such as culls. While porcine zona pellucida (PZP) effectively achieves female contraception in several mammalian species, its effects on behavior and subsequent physiology can be extensive. Feral horses form stable social groups (or bands), consisting of (usually) one male (stallion), several females (mares), and their offspring (foals). My research on the feral horses of Shackleford Banks, NC, USA, showed that mares receiving PZP 1) were up to 10 times as likely to switch bands, 2) visited approximately twice as many groups, and 3) both demonstrated and received increased reproductive interest (to/from the stallion). In a gregarious species like the horse, such changes could have serious consequences..
Nuñez, C.M.V., J.S. Adelman, C. Mason, and D.I. Rubenstein. 2009. Immunocontraception decreases group fidelity in a feral horse population during the non-breeding season. Applied Animal Behaviour Science, 117: 74-83.
Feral horse populations have expanded across the United Sates, making them the subject of considerable controversy. The extirpation of their natural predators and land use conflicts with humans all but necessitate some form of population management wherever feral horses occur. Given the options, contraception appears the most humane, providing population control, while avoiding more invasive measures such as culls. While porcine zona pellucida (PZP) effectively achieves female contraception in several mammalian species, its effects on behavior and subsequent physiology can be extensive. Feral horses form stable social groups (or bands), consisting of (usually) one male (stallion), several females (mares), and their offspring (foals). My research on the feral horses of Shackleford Banks, NC, USA, showed that mares receiving PZP 1) were up to 10 times as likely to switch bands, 2) visited approximately twice as many groups, and 3) both demonstrated and received increased reproductive interest (to/from the stallion). In a gregarious species like the horse, such changes could have serious consequences..
Nuñez, C.M.V., J.S. Adelman, C. Mason, and D.I. Rubenstein. 2009. Immunocontraception decreases group fidelity in a feral horse population during the non-breeding season. Applied Animal Behaviour Science, 117: 74-83.
Contraception and reproductive cycling
My research has shown that since the contraception program on Shackleford Banks, NC, began in January 2000, foaling has occurred over a significantly broader range than it had before the contraception program. Moreover, after the contraception program was instituted, foaling in PZP recipients occurred over a broader range than did foaling in non-recipients. In addition, current recipients of PZP foaled later in the year than did prior recipient and non-recipient mares. Females receiving more consecutive PZP applications gave birth later in the season than did females receiving fewer applications. Finally, the efficacy of PZP declined with increasing consecutive applications before reaching 100% after five consecutive applications. For a gregarious species such as the horse, the extension of reproductive cycling into the fall months has important social consequences, including decreased group stability and the extension of male reproductive behavior. In addition, reproductive cycling into the fall months could have long-term effects on foal survivorship. Managers should consider these factors before enacting contraceptive programs in new populations. My research suggests that even minor alterations to management strategies can help alleviate such unintended effects in new populations.
Nuñez, C.M.V., J.S. Adelman, and D.I. Rubenstein. 2010. Immunocontraception in wild horses (Equus caballus) extends reproductive cycling beyond the normal breeding season. PLOS ONE, 5(10): e13635.
My research has shown that since the contraception program on Shackleford Banks, NC, began in January 2000, foaling has occurred over a significantly broader range than it had before the contraception program. Moreover, after the contraception program was instituted, foaling in PZP recipients occurred over a broader range than did foaling in non-recipients. In addition, current recipients of PZP foaled later in the year than did prior recipient and non-recipient mares. Females receiving more consecutive PZP applications gave birth later in the season than did females receiving fewer applications. Finally, the efficacy of PZP declined with increasing consecutive applications before reaching 100% after five consecutive applications. For a gregarious species such as the horse, the extension of reproductive cycling into the fall months has important social consequences, including decreased group stability and the extension of male reproductive behavior. In addition, reproductive cycling into the fall months could have long-term effects on foal survivorship. Managers should consider these factors before enacting contraceptive programs in new populations. My research suggests that even minor alterations to management strategies can help alleviate such unintended effects in new populations.
Nuñez, C.M.V., J.S. Adelman, and D.I. Rubenstein. 2010. Immunocontraception in wild horses (Equus caballus) extends reproductive cycling beyond the normal breeding season. PLOS ONE, 5(10): e13635.
How quickly do mares exhibit behavioral and physiological recovery from different levels of contraception management?
One of the presumed advantages of porcine zona pellucida (PZP) is its reversibility. We showed that after six years without treatment, previously treated mares remained largely infertile, continued to cycle later into the calendar year, and were more likely to leave their band for another. These effects were exacerbated in mares that had previously received more treatments; mares receiving fewer treatments exhibited more natural behaviors. Our results suggest that although PZP-induced infertility and its associated physiological and behavioral effects can persist after treatment cessation, these effects can be reduced. Our work reiterates that careful consideration to the number of years females are kept infertile is important if managers are to maintain more naturally functioning populations. In addition, our results show that the ability to manage populations adaptively may be compromised if females are kept infertile for extended periods of time.
Nuñez, C.M.V., J.S. Adelman, H.A. Carr*, C.M. Alvarez*, D.I. Rubenstein. 2017. Lingering effects of contraception management on feral mare (Equus caballus) fertility and social behavior. Conservation Physiology, 5(1): cox018.
One of the presumed advantages of porcine zona pellucida (PZP) is its reversibility. We showed that after six years without treatment, previously treated mares remained largely infertile, continued to cycle later into the calendar year, and were more likely to leave their band for another. These effects were exacerbated in mares that had previously received more treatments; mares receiving fewer treatments exhibited more natural behaviors. Our results suggest that although PZP-induced infertility and its associated physiological and behavioral effects can persist after treatment cessation, these effects can be reduced. Our work reiterates that careful consideration to the number of years females are kept infertile is important if managers are to maintain more naturally functioning populations. In addition, our results show that the ability to manage populations adaptively may be compromised if females are kept infertile for extended periods of time.
Nuñez, C.M.V., J.S. Adelman, H.A. Carr*, C.M. Alvarez*, D.I. Rubenstein. 2017. Lingering effects of contraception management on feral mare (Equus caballus) fertility and social behavior. Conservation Physiology, 5(1): cox018.
Effects to close associates
In social species like the feral horse, changes in individual behavior are likely to impact associated animals. My former Masters student, Maggie Jones (now earning her PhD at The University of Florida at Gainnesville), compared the frequency of male-male contests for males that experienced varying levels of mare group changing behavior. She found that males experiencing more group changes (either into or out of their bands) spent more time vigilant, fought more often, and that their fights were more highly escalated than were males experiencing fewer group changes.
Jones, M.M.** and C.M.V. Nuñez. 2019. Decreased mare fidelity alters stallion behavior in a population managed with immunocontraception. Applied Animal Behaviour Science 214: 34-41.
Moreover, when tested experimentally via audio playback, males experiencing more group changes were 1) more likely to respond to playback calls and 2) took longer to return to previous/normal behaviors after playback, further supporting the link between mare group changing behavior and male aggression.
Jones, M.M.** and C.M.V. Nuñez. 2020. Rising up to the challenge of their rivals: Mare infidelity intensifies stallion response to playback of aggressive conspecific vocalizations. Applied Animal Behaviour Science, 225: 104949.
Surprisingly, these changes did not seem to affect male stress physiology, even though similar behaviors are commonly associated with increases in cortisol (a steroid hormone typically produced in response to physical or social challenges) in other species. Our work highlights the importance of considering both physiological and
behavioral measures when investigating animal responses to challenging situations. Only by using
such a holistic approach can we best understand the potential costs animals face; this is especially
important in managed populations in which human perturbation can lead to unintended side effects.
Jones, M.M.** and C.M.V. Nuñez. 2023. Laissez-Faire Stallions? Males’ Fecal Cortisol Metabolite
Concentrations Do Not Vary with Increased Female Turnover in Feral Horses (Equus caballus). Animals, 13,176.
These results are important as they 1) demonstrate the potential for PZP-induced changes in recipient animals to affect non-recipient behavior and potentially stress physiology and 2) increase our understanding of how contraceptive management may impact non-target animals.
Jones, M.M.** and C.M.V. Nuñez. 2019. Decreased mare fidelity alters stallion behavior in a population managed with immunocontraception. Applied Animal Behaviour Science 214: 34-41.
Moreover, when tested experimentally via audio playback, males experiencing more group changes were 1) more likely to respond to playback calls and 2) took longer to return to previous/normal behaviors after playback, further supporting the link between mare group changing behavior and male aggression.
Jones, M.M.** and C.M.V. Nuñez. 2020. Rising up to the challenge of their rivals: Mare infidelity intensifies stallion response to playback of aggressive conspecific vocalizations. Applied Animal Behaviour Science, 225: 104949.
Surprisingly, these changes did not seem to affect male stress physiology, even though similar behaviors are commonly associated with increases in cortisol (a steroid hormone typically produced in response to physical or social challenges) in other species. Our work highlights the importance of considering both physiological and
behavioral measures when investigating animal responses to challenging situations. Only by using
such a holistic approach can we best understand the potential costs animals face; this is especially
important in managed populations in which human perturbation can lead to unintended side effects.
Jones, M.M.** and C.M.V. Nuñez. 2023. Laissez-Faire Stallions? Males’ Fecal Cortisol Metabolite
Concentrations Do Not Vary with Increased Female Turnover in Feral Horses (Equus caballus). Animals, 13,176.
These results are important as they 1) demonstrate the potential for PZP-induced changes in recipient animals to affect non-recipient behavior and potentially stress physiology and 2) increase our understanding of how contraceptive management may impact non-target animals.
