Female Barbary macaques implanted with the contraceptive Implanon exhibited behaviors indicating higher anxiety levels, such as increased self-scratching and self-grooming, compared to females without implants. They also showed more aggression and spent more time traveling while spending less time resting and giving grooming. There were no significant differences in foraging behavior between groups. These results suggest Implanon implantation had multiple effects on behavior in female Barbary macaques.

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Investigating Potential Effects of the Contraceptive
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Female Barbary Macaques
Amanda M. Maijer & Stuart Semple
To cite this article: Amanda M. Maijer & Stuart Semple (2015): Investigating Potential Effects of
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Journal of Applied Animal Welfare Science, DOI: 10.1080/10888705.2015.1083432
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2. Investigating Potential Effects of the Contraceptive Implanon on the
Behavior of Free-Ranging Adult Female Barbary Macaques
Amanda M. Maijer and Stuart Semple
Centre for Research in Evolutionary and Environmental Anthropology, University of Roehampton, London,
United Kingdom
ABSTRACT
In recent years, the use of hormonal contraception in captive, free-ranging,
and wild mammal populations has increased, but the effects on these
nonhuman animals’ behavior and the associated welfare impacts remain
poorly understood. This study of free-ranging adult female Barbary macaques
(Macaca sylvanus) at Trentham Monkey Forest compared females implanted
with the progestin-only contraceptive Implanon to those not receiving
contraception. Females with contraceptive implants had higher rates of self-
scratching and spent more time self-grooming (2 behavioral indexes of
anxiety) than those without implants. They also directed more aggression at
others, spent more time receiving grooming and traveling, and spent less
time giving grooming and resting. No significant differences between the 2
groups of females were seen for time spent foraging. These results suggest
that Implanon had a number of effects on Barbary macaques, although these
need to be considered in light of the significant benefits afforded by the
use of this contraceptive. The findings of this study provide important
information to those evaluating the relative welfare costs and benefits of
alternative methods of population control in this and other species.
KEYWORDS
Behavior; welfare; contra-
ception; anxiety; stress
For many mammals in captivity, excellent husbandry conditions lead to high reproductive rates and
populations rapidly outgrowing the available space (Asa, 1997). Moreover, many species of mammals in
the wild increasingly share space with human populations and flourish in such environments, leading
to rapid population increases and calls to restrict their numbers (Asa & Porton, 2005). Initially, lethal
control and surgical sterilization were the predominant methods used to control such nonhuman
animal populations, but these techniques are costly and logistically challenging and can have a range
of undesirable welfare consequences (Gray & Cameron, 2010; Kirkpatrick, 2007). More recently,
hormonal contraception has become a popular method to control animal population size (Asa, 2005;
Gray & Cameron, 2010). This approach has been primarily adopted in captive settings (Asa, Porton, &
Calle, 2005; Porton & Dematteo, 2005), but it is also used in free-ranging and wild populations
(Kirkpatrick & Frank, 2005).
The use of hormonal contraceptives in captive and noncaptive mammals gives rise to a number of
concerns, however. When capture is necessary to implant a contraceptive device, it may result in stress
to the individuals concerned and disruption to the social structure of the group (Munson, Moresco, &
Calle, 2005). Even when capture is not needed, or after this event has taken place when it is required, the
biological action of the contraception may have negative welfare impacts (Asa et al., 2005; Munson
et al., 2005). In particular, changes in levels of sex steroids brought about by many hormonal
contraceptives could potentially negatively affect emotional states—and therefore psychological well
being—of the animals in question and/or may modify their behaviors in ways that detrimentally affect
q 2015 Taylor & Francis
CONTACT Stuart Semple s.semple@roehampton.ac.uk Centre for Research in Evolutionary and Environmental Anthropology,
University of Roehampton, Holybourne Avenue, London SW15 4JD, United Kingdom.
JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE
http://dx.doi.org/10.1080/10888705.2015.1083432
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3. their welfare. Ultimately, the decision to implement hormonal contraception in mammals must be
based on an analysis of the costs and benefits of this method of population control and of the alternative
options (Kirkpatrick, 2007). Detailed information on the effects of hormonal contraception is key to
this decision process but is so far very limited.
Sex steroids can have potent effects on emotional states in humans, with female sex hormones being
linked in particular to increased anxiety (Toufexis, Myers, & Davis, 2006). It has been known for more
than 40 years that the use of hormonal contraceptives can cause negative changes in women’s moods
(Cullberg, 1972; Poromaa & Segebladh, 2012), but the impact of contraception on emotional states in
nonhuman animals remains a neglected area of research (Gray & Cameron, 2010). To our knowledge,
only one study to date has attempted to explore this issue. Plowman, Jordan, Anderson, Condon,
and Fraser (2004) tested zoo-housed hamadryas baboons (Papio hamadryas) for potential negative
psychological effects of Norplant, an implanted contraceptive with an active ingredient with
progesterone-like activity. To do so, they measured the rate of self-directed behaviors, which provides a
useful index of anxiety in humans and nonhuman primates (Maestripieri, Schino, Aureli, & Troisi,
1992; Schino, Perretta, Taglioni, Monaco, & Troisi, 1996). No evidence was found for a change in self-
directed behavior rates linked to contraception use, but as the authors acknowledged, changes in group
size during their study might have masked any such effects.
Evidence that hormonal contraception increases levels of aggressive behavior has been found in
captive long-tailed macaques (Henderson & Shively, 2004) and pigtail macaques (Pazol, Wilson, &
Wallen, 2004). Such effects are of clear welfare concern, as elevated rates of aggression increase the risk
for physical injury and disrupt normal patterns of social organization (Penfold, Patton, & Jochle, 2005).
There is also evidence from captive populations of a range of mammal species—such as white-tailed
deer (Bertrand, DeNicola, Beissinger, & Swihart, 1996), long-tailed macaques (Shively, Manuck,
Kaplan, & Koritnik, 1990), and golden-headed lion tamarins (De Vleeschouwer, Leus, & Van Elsacker,
2000)—that hormonal contraceptives decrease rates of affiliative behavior. These effects are also
important when assessing welfare impacts, as there is evidence that sociopositive behaviors such as
grooming can reduce anxiety and physiological stress levels (Crockford et al., 2008; Shutt, MacLarnon,
Heistermann, & Semple, 2007; Yates & Aureli, 2010).
In this study, we explored potential impacts of the progestin-only contraceptive Implanon in free-
ranging, adult female Barbary macaques. We tested whether there were differences between females
with and without Implanon implants with respect to behavioral indexes of anxiety (self-directed
behaviors) and measures of aggression and affiliation. To allow for comparison with the broadest range
of previous studies of contraception in animals, in which impacts on general activity patterns were
frequently assessed (Gray & Cameron, 2010), we also tested for potential effects on three measures of
activity: traveling, foraging, and resting. Hormonal contraception is used in both free-ranging (Wallner,
Möstl, & Dittami, 2007) and wild populations (Cortes & Shaw, 2006) of our study species and in a
range of other mammal species in captive, free-ranging, and wild settings (Gray & Cameron, 2010).
Our findings will therefore provide valuable information to those evaluating the relative costs and
benefits of alternative methods of population control in Barbary macaques and other species.
Materials and methods
Study site and animals
We studied the behavior of 20 adult, female Barbary macaques (age range ¼ 5–17 years) living in one
group of the free-ranging population at Trentham Monkey Forest in Stoke-on-Trent, United Kingdom.
The total troop size was 73 individuals: 24 subadult or adult males, 28 subadult or adult females, 16
juveniles, and 5 infants. Barbary macaques live in multimale/multifemale groups characterized by
female philopatry and male dispersal, with close bonds between matrilineal kin (Paul & Kuester, 1987;
Silk, 1987). Of the focal females, 13 were on the progestin-only contraceptive implant Implanon,
which had been administered 1 year to 4 years prior to the start of this study; this implant has been
2 MAIJER AND SEMPLE
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4. found to be effective at preventing pregnancy for at least 4 years in this population (S. Wiper, personal
communication, March 14, 2013). Implanon releases the progestin etonogestrel (Bennink, 2000;
Croxatto, 2002). It functions by partially or completely inhibiting ovulation via suppression of midcycle
luteinizing hormone peaks by causing thickening of the cervical mucus, which prevents sperm from
meeting the egg, and by thinning of the endometrium, which prevents implantation (Croxatto &
Makarainen, 1998; Varma & Mascarenhas, 2001).
The researchers did not know the contraception status of each focal female at the start of the
observation period, and their status remained unknown throughout the study except for the five
females who did not have contraceptive implants and gave birth. The selection of females for
contraception was based on a range of factors including their reproductive histories, the sizes of their
matrilines, and how many closely related females were on contraception. Although this was not a truly
random selection process, we did not think it would lead to biases that would affect our study.
In support of this, we found that females with and without contraceptive implants did not differ
significantly in age—analysis of variance (ANOVA), F(1, 18) ¼ 3.045, p ¼ .098—or in dominance
rank—ANOVA, F(1, 18) ¼ 1.154, p ¼ .297—as assessed from a matrix of the outcomes of dyadic
agonistic interactions.
Data collection
The protocol for this project was approved by the Roehampton University Ethics Committee and by
Trentham Monkey Forest. Behavioral data (220 hr total, 11 hr per female) were collected from April 18,
2011, to June 8, 2011, during 15-min continuous focal observations using a Teklogix Psion handheld
computer loaded with Noldus Observer 5 software. The order of focal samples was randomized to
ensure that they were distributed evenly across the day for each female. The data collection period was
after the end of the breeding season, which ends in late January.
We recorded the duration of time spent giving and receiving grooming, self-grooming, traveling,
foraging, and resting. In addition, we recorded the frequency of occurrence of self-scratching (with
separate bouts of self-scratching defined by a break of 3 s or more) and the frequency of occurrence of
aggression (threats, chasing, contact, and biting). For any observations where the focal animal was out
of sight for more than 2 min, the observation was discontinued and discarded and another female was
followed; the original female was followed again at the next available opportunity.
Statistical analysis
The time that the focal animal was out of sight in a focal observation was subtracted from the total
observation time to determine the duration that the animal was in view for that observation. These
values were used to calculate for each focal observation the rates of self-scratching and of aggression
per hour and percentage time engaged in foraging, resting, traveling, giving and receiving grooming,
and self-grooming. For each female, a mean was then calculated across all focal watches for each
behavior. Initial analyses indicated no significant differences in behavior between females not on
contraception who did and did not give birth (Mann Whitney tests, all p . .095), so these females
were grouped together for comparison with the group of females with contraceptive implants.
Data were found to be normally distributed, so ANOVAs were used to compare rates or durations
of behavior between females on contraception and those not on contraception. As both pregnancy
and the birth of an infant may affect females’ behaviors, we then repeated all analyses using, for the
five females who gave birth, (a) only data from before birth of the infant and (b) only data after the
birth of the infant. Only four results differed with respect to significance between the analyses using
the complete data set and those using data from only before, or only after, birth. For brevity, we
report here only the results for the complete data set but highlight the instances where the significance
of the result changed when using one of the restricted data sets. Analyses were carried out in the
EFFECTS OF IMPLANON ON MACAQUE BEHAVIOR 3
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5. Statistical Package for the Social Sciences Version 17.0. All statistical tests were two-tailed,
with a ¼ .05.
Results
The rates and time spent in each behavior for females with and without Implanon contraceptive
implants are shown inTable 1. Compared with females not on contraception, females with implants had
significantly higher rates of self-scratching—ANOVA, F(1, 18) ¼ 20.878, p , .001—and giving
aggression—ANOVA, F(1, 18) ¼ 7.490, p ¼ .014—and spent more time self-grooming—ANOVA, F(1,
18) ¼ 12.365, p ¼ .002—receiving grooming—ANOVA, F(1, 18) ¼ 13.365, p ¼ .002—and traveling—
ANOVA, F(1, 18) ¼ 21.158, p , .001. Females on contraception also spent less time giving grooming—
ANOVA, F(1, 18) ¼ 4.502, p ¼ .048—and less time resting—ANOVA, F(1, 18) ¼ 6.765, p ¼ .018—than
did females not on contraception. There were no significant differences between the two groups of
females with respect to time spent foraging—ANOVA, F(1, 18) ¼ 1.043, p ¼ .321.
The difference in resting time between the two groups of females was no longer significant when, for
those females who gave birth, only the behavioral data after the birth of infants were included—
ANOVA, F(1, 18) ¼ 2.146, p ¼ .160. Similarly, the difference in the amount of grooming received
was no longer significant when only postbirth data were analyzed for these females—ANOVA, F(1,
18) ¼ 2.416, p ¼ .138. Finally, the difference in the amount of grooming given was not significant when
only data before—ANOVA, F(1, 17) ¼ 0.130, p ¼ .723—or after—ANOVA, F(1, 18) ¼ 0.542, p ¼ .471
—birth were considered for those females who gave birth.
Discussion
In this study, we compared the behavior of free-ranging, adult female Barbary macaques implanted
with the progestin-only contraceptive Implanon with others in the same group who were not on
contraception. Females with the contraceptive implant showed higher rates of two behavioral indexes
of anxiety—self-scratching and self-grooming—and were also more frequently aggressive toward
conspecifics. There was evidence that affiliative behavior was also affected by the implant: Females on
contraception gave less and received more grooming than did females not on contraception.
In addition, some aspects of general activity appeared to be altered by Implanon: Being on this
contraception was linked to increased traveling and reduced resting times, but foraging time was not
affected.
Both the rate of self-scratching and the proportion of time spent self-grooming were markedly
higher among females with Implanon implants, indicating that females on contraception may have
higher average anxiety levels than those not on contraception. This finding is in line with studies in the
human literature indicating that hormonal contraception can have negative effects on mood (Poromaa
& Segebladh, 2012). However, in such studies, the prevalence of such effects tends to be low, with
Table 1. Rates or time spent in each behavior for females with and without Implanon implants.
Behavior
Females with Implanon
implant (n ¼ 13)
Females without Implanon
implant (n ¼ 7)
Difference between
groups
Self-scratching (bouts/hr) 14.76 ^ 2.85 (11.09 2 20.36) 8.56 ^ 2.98 (3.60 2 10.78) ***
Self-grooming (% time) 1.93 ^ 0.80 (0.77 2 3.27) 0.73 ^ 0.55 (0.11 2 1.67) **
Giving grooming (% time) 4.71 ^ 2.66 (1.35 2 8.91) 7.66 ^ 3.52 (2.01 2 12.69) *
Being groomed (% time) 13.47 ^ 3.56 (6.54 2 20.08) 7.08 ^ 4.03 (2.27 2 12.96) **
Aggression given (bouts/hr) 2.12 ^ 1.11 (0.59 2 4.28) 0.84 ^ 0.67 (0.36 2 2.32) *
Travel (% time) 16.69 ^ 2.91 (10.84 2 21.30) 9.89 ^ 3.58 (6.87 2 17.07) ***
Forage (% time) 26.40 ^ 3.70 (20.0 2 32.16) 29.13 ^ 8.23 (19.13 2 42.86) ns
Rest (% time) 34.46 ^ 4.75 (24.59 2 42.83) 44.45^12.51 (23.68 2 57.30) *
Note. Numbers indicate mean ^1 SD, with the range given in parentheses. Differences between the two groups of females are
indicated in the final column, where * p , .05, ** p , .01, *** p , .001, and ns ¼ not significant.
4 MAIJER AND SEMPLE
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6. between 4% and 10% of individuals reporting effects. A similar low frequency of effect in the present
study would almost certainly have precluded any detection of significant differences; the statistically
highly significant link between contraception and increased indexes of anxiety in our study suggests
that effects on emotional state may be more common in Barbary macaques than in humans.
However, the apparently negative impacts of Implanon on anxiety in the current study need to be
interpreted with caution. First, as is the case for all of the results presented in this study, the nature of
our analyses precludes robust inference of causality. Second, evidence from rodents (Berridge, Mitton,
Clark, & Roth, 1999; Hennessy & Foy, 1987; Hori, Yuyama, & Tamura, 2004) and humans
(Mohiyeddini & Semple, 2012; Pico-Alfonso et al., 2007) has suggested that self-directed behaviors
represent effective strategies for coping with short-term, negative shifts in emotional states; thus,
elevated rates of such behavior may not translate into detrimental, long-term, or physiological impacts
if this coping function is effective. Third, it is possible that contraception increases skin sensitivity and
irritation in monkeys, as happens in humans (Jelinek, 1970); this may lead to an increase in self-
scratching and self-grooming that is unrelated to anxiety, thus making these self-directed behaviors less
reliable as indicators of how anxious an animal is.
Females with Implanon implants more frequently directed aggression at other group members than
did those without implants. This may be due to the underlying changes in reproductive hormones that
Implanon produces. Progestins are antagonistic to androgens, and this may lead to important behavioral
changes in animals fitted with contraceptive implants such as Implanon. Pazol et al. (2004) found
evidence that the steroidal progestin medroxyprogesterone acetate (MPA) antagonizes the effects of
estradiol in female pigtail macaques. In their study, ovariectomized females given estradiol showed
a trend toward lower levels of aggression compared with control females; by contrast, females given
estradiol and MPA showed markedly higher rates of aggression compared with controls. Thus,
progestin-based contraception may interfere with the sociopositive effects of female reproductive
hormones (Pazol et al., 2004). Future investigations of the effects of contraception in captive or wild
animals will benefit from exploring the interaction between androgen levels and patterns of aggressive
and other types of behaviors; unfortunately, endocrinological analyses of this kind were beyond the scope
of the present study.
We found evidence linking contraception to patterns of grooming: Females with the implants spent
less time grooming and more time being groomed compared with females not on the contraception.
There is evidence that receiving grooming lowers heart rate (Aureli, Preston, & de Waal, 1999; Boccia,
Laudenslager, & Reite, 1989) and leads to endorphin release (Keverne, Martensz, & Tuite, 1989), and
thus, it may have an important calming effect. If animals on contraception are more anxious, they may
therefore solicit grooming from others to regulate their emotional states.
Additionally, such animals may be less inclined to approach other animals to groom them due to
their anxiety. In support of this idea, Shutt et al. (2007) found a negative relationship between
physiological stress levels and both the amount of grooming given away and the number of females to
whom it was given among female Barbary macaques, potentially indicating that more stressed animals
are less likely to groom others. In this and other primate species, grooming is a key behavior in social
bonding (Dunbar, 1988) and is also “traded” for other services such as coalitionary support (Carne,
Wiper, & Semple, 2011); the apparent impact of contraception on the balance of giving and receiving
grooming may therefore have important implications for the social relationships within the group.
For females on contraception, time spent traveling was significantly higher and time spent resting
was lower. A similar increase in time spent moving was seen in a study of the effects of oral
contraceptive administration in captive long-tailed macaques (Macaca fascicularis; Henderson &
Shively, 2004). By contrast, there was no difference in foraging time between females with and without
the Implanon implant, although as the study population was provisioned, foraging time was greatly
reduced compared with the wild populations, and energy demands could be met in a shorter time
period. Any potential differences in foraging time among females with and without contraception—for
example, due to increased energetic expenditure as a result of increased traveling and reduced resting
time—may be hard to detect.
EFFECTS OF IMPLANON ON MACAQUE BEHAVIOR 5
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7. Some of the differences in behavior we found linked to contraception were no longer significant
when, for the females who gave birth, only data from before birth of the infant or after the birth of the
infant were analyzed. Unfortunately, the small number of such females—five in total—meant we were
unable to explore whether this was a biologically meaningful effect or rather the result of reduced
statistical power.
Conclusion
Overall, our findings provide evidence that the contraceptive Implanon may have a number of effects
on the behavior of free-ranging, adult, female Barbary macaques; such effects may also be seen when
other forms of chemical contraception manipulating reproductive hormone levels (e.g., oral
contraceptives) are used. It is crucial that the changes in behavior that we found, while potentially
indicative of undesirable impacts, be considered carefully in the light of two key factors. First, it is
unclear whether the magnitude of the behavioral changes found is biologically meaningful in terms of
affecting welfare; studies incorporating cognitive and physiological measures would be needed to
determine whether changes in grooming, aggression, or self-directed behaviors may translate into
psychologically or physically deleterious impacts. Second, it is important to consider the behavioral
impacts of contraception not in isolation, but rather within the framework of all the other potential
means of effective population control (Kirkpatrick, 2007). This holistic evaluation of the relative costs
and benefits of all available options should be underpinned by rigorous data. The findings of the current
study contribute to the growing database on the effects of contraception in wildlife that will be crucial in
these types of decision making.
Acknowledgments
We sincerely thank Sue Wiper and Guillaume and Sophie de Turckheim for allowing us to work at Trentham Monkey
Forest. Frimpong Twum provided expert technical support. We thank also Charlotte Carne and Ann MacLarnon for their
thoughtful comments on an earlier draft of this manuscript.
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