Postpartum cessation of urban space use by a female baboon living at the edge of the City of Cape Town

Species with slow life history strategies that invest in few offspring with extended parental care need to adapt their behavior to cope with anthropogenic changes that occur within their lifetime. Here we show that a female chacma baboon (Papio ursinus) that commonly ranges within urban space in the City of Cape Town, South Africa, stops using urban space after giving birth. This change of space use occurs without any significant change in daily distance traveled or social interactions that would be expected with general risk-sensitive behavior after birth. Instead, we suggest this change occurs because of the specific and greater risks the baboons experience within the urban space compared to natural space, and because leaving the troop (to enter urban space) may increase infanticide risk. This case study can inform methods used to manage the baboons' urban space use in Cape Town and provides insight into how life history events alter individuals' use of anthropogenic environments

“Micropersonality” traits and their implications for behavioral and movement ecology research

Many animal personality traits have implicit movement‐based definitions and can directly or indirectly influence ecological and evolutionary processes. It has therefore been proposed that animal movement studies could benefit from acknowledging and studying consistent interindividual differences (personality), and, conversely, animal personality studies could adopt a more quantitative representation of movement patterns. Using high‐resolution tracking data of three‐spined stickleback fish (Gasterosteus aculeatus), we examined the repeatability of four movement parameters commonly used in the analysis of discrete time series movement data (time stationary, step length, turning angle, burst frequency) and four behavioral parameters commonly used in animal personality studies (distance travelled, space use, time in free water, and time near objects). Fish showed repeatable interindividual differences in both movement and behavioral parameters when observed in a simple environment with two, three, or five shelters present. Moreover, individuals that spent less time stationary, took more direct paths, and less commonly burst travelled (movement parameters), were found to travel farther, explored more of the tank, and spent more time in open water (behavioral parameters). Our case study indicates that the two approaches—quantifying movement and behavioral parameters—are broadly equivalent, and we suggest that movement parameters can be viewed as “micropersonality” traits that give rise to broad‐scale consistent interindividual differences in behavior. This finding has implications for both personality and movement ecology research areas. For example, the study of movement parameters may provide a robust way to analyze individual personalities in species that are difficult or impossible to study using standardized behavioral assays

Dynamics of collective motion across time and species

Most studies of collective animal behaviour rely on short-term observations, and comparisons of collective behaviour across different species and contexts are rare. We therefore have a limited understanding of intra- and interspecific variation in collective behaviour over time, which is crucial if we are to understand the ecological and evolutionary processes that shape collective behaviour. Here, we study the collective motion of four species: shoals of stickleback fish (Gasterosteus aculeatus), flocks of homing pigeons (Columba livia), a herd of goats (Capra aegagrus hircus) and a troop of chacma baboons (Papio ursinus). First, we describe how local patterns (inter-neighbour distances and positions), and group patterns (group shape, speed and polarization) during collective motion differ across each system. Based on these, we place data from each species within a ‘swarm space’, affording comparisons and generating predictions about the collective motion across species and contexts. We encourage researchers to add their own data to update the ‘swarm space’ for future comparative work. Second, we investigate intraspecific variation in collective motion over time and provide guidance for researchers on when observations made over different time scales can result in confident inferences regarding species collective motion. This article is part of a discussion meeting issue ‘Collective behaviour through time’

You Mate, I Mate: Macaque Females Synchronize Sex not Cycles

Extended female sexuality in species living in multimale-multifemale groups appears to enhance benefits from multiple males. Mating with many males, however, requires a low female monopolizability, which is affected by the spatiotemporal distribution of receptive females. Ovarian cycle synchrony potentially promotes overlapping receptivity if fertile and receptive periods are tightly linked. In primates, however, mating is often decoupled from hormonal control, hence reducing the need for synchronizing ovarian events. Here, we test the alternative hypothesis that females behaviorally coordinate their receptivity while simultaneously investigating ovarian cycle synchrony in wild, seasonal Assamese macaques (Macaca assamensis), a promiscuous species with extremely extended female sexuality. Using fecal hormone analysis to assess ovarian activity we show that fertile phases are randomly distributed, and that dyadic spatial proximity does not affect their distribution. We present evidence for mating synchrony, i.e., the occurrence of the females' receptivity was significantly associated with the proportion of other females mating on a given day. Our results suggest social facilitation of mating synchrony, which explains (i) the high number of simultaneously receptive females, and (ii) the low male mating skew in this species. Active mating synchronization may serve to enhance the benefits of extended female sexuality, and may proximately explain its patterning and maintenance

Reproductive and Life History Parameters of Wild Female Macaca assamensis

Information on basic reproductive parameters and life-history traits is crucial for the understanding of primate evolution, ecology, social behavior, and reproductive strategies. Here, we report 4 yr of data on reproductive and life-history traits for wild female Assamese macaques (Macaca assamensis) at Phu Khieo Wildlife Sanctuary, northeastern Thailand. During 2 consecutive reproductive seasons, we investigated reproductive behavior and sexual swelling size in 16 females and collected 1832 fecal samples. Using enzyme immunoassays, we measured fecal estrogen and progesterone metabolites to assess ovarian activity and timing of ovulation and to ascertain conceptions and pregnancies. Timing of reproduction was strictly seasonal (births: April–July, 86% in April–June, 4 yr, n = 29; conceptions: October–February, 65% in December–January, 2 yr, n = 17). Females showed no cyclic ovarian activity outside the mating season and conceived in their first or second cycle (mean: 1.2 cycles to conception, n = 13). Gestation length was on average 164.2 d (range: 158–170, n = 10), and females had their first infant at an age of 5 yr (n = 4). Interbirth intervals were bimodally distributed, with females giving birth on average every 13.9 or 23.2 mo. Shorter interbirth intervals were linked to early parturition within the birth season. Most females displayed subcaudal sexual swellings which, however, did not reliably indicate female reproductive status or fertility. Overall, our results fall within the range of findings reported for other macaque species. These results thus add to the growing body of information available for wild macaques, facilitating comparative studies for a better understanding of interspecific differences in social and reproductive patterns

Die Sozio-Endokrinologie weiblicher Fortpflanzungsstrategien bei freilebenden Assammakaken (Macaca assamensis)

Sexueller Konflikt ist ein typisches Merkmal von Tieren in gemischten Geschlechtergruppen, und treibt die Evolution von geschlechtsspezifischen Reproduktionsstrategien. Aufgrund divergierender reproduktiver Optima, sollten Männchen untereinander konkurrieren, um möglichst viele Weibchen zu monopolisieren und sich mit ihnen zu paaren. Im Gegensatz dazu sollten Weibchen ihre Partner selektiv auswählen. Dies führt zu einem koevolutionären Wettstreit zwischen den Geschlechtern. Das potentielle Risiko von Infantizid durch Männchen kreiert ein Dilemma für Weibchen. Um das Infantizidrisiko zu verringern und die Vaterschaft gleichzeitig zu konzentrieren und zu verschleiern, entwickeln Weibchen Gegenstrategien und Mechanismen, die das Monopolisierungspotential der Männchen (d.h. den male mating-skew) herabsetzen und deren Abschätzungen der Vaterschaftswahrscheinlichkeit manipulieren. Das Ziel dieser Dissertation war es, weibliche Reproduktionsstrategien und deren zugrundeliegende proximate Mechanismen eines Primaten mit geringer direkter Konkurrenz unter Männchen, dem Assammakaken (Macaca assamensis), zu untersuchen. Durch eine Kombination von Verhaltensbeobachtungen, demographischen, und Hormondaten, konnten generelle weibliche Reproduktionsparameter und life-history Merkmale untersucht werden. Zusätzlich wurden Größenveränderungen in Anogenitalschwellungen dokumentiert, um deren funktionelle Bedeutung zu bestimmen. Die sexuelle Aktivität der Weibchen und ihre consortships mit Männchen wurden in Relation zur Fertilität gesetzt. Desweiteren wurden die zeitliche Verteilung und Überlappung von fertilen Phasen untersucht, und eine neue Hypothese, dass Weibchen ihre Paarungsaktivität unabhängig von hormonellem Einfluss synchronisieren, aufgestellt und getestet. Die Studie wurde in zwei aufeinanderfolgenden Paarungszeiten (07/08 und 08/09) im Phu Khieo Wildlife Sanctuary im Nordosten Thailands durchgeführt. Von 16 Weibchen einer freilebenden, habituierten Gruppe von 50-60 Individuen wurden Fokustier- (> ;800 Stunden) und ad libitum-Daten erhoben. Darüber hinaus wurden über 2300 Kotproben gesammelt, um mit Hilfe von Enzym-Immuno-Assays (EIA) für Östrogen-, Gestagen- und Androgenmetabolite Zyklus- und Schwangerschaftscharakteristika zu beschreiben und Ovulationen und Konzeptionen zu bestimmen. Die endokrinen Profile zeigten, dass es möglich ist, den Reproduktionsstatus von Assammakakenweibchen mittels non-invasiver Methoden zu charakterisieren. Die Muster fäkaler Ausscheidung von Androgenen erlauben eine frühe Schwangerschaftserkennung und eine pränatale Geschlechtsbestimmung des Fötus. Die Tragzeit und das Intergeburtenintervall fielen in den Bereich nahe verwandter Arten. Außerhalb der Paarungszeit waren Weibchen anovulatorisch und konzipierten meist im ersten Ovulationszyklus innerhalb der 4-monatigen Paarungszeit. 65% aller Konzeptionen fanden im Dezember und Januar statt. Die unauffälligen subkaudalen Sexualschwellungen signalisierten nicht die Ovulationswahrscheinlichkeit, und die Weibchen zeigten keine Kopulationsrufe oder Anzeichen von Verhaltensöstrus. Dies weist auf eine verschleierte Fertilität bei Weibchen dieser Art hin. Demgemäß standen die langen consortships mit hochrangigen Männchen in keinem direkten Zusammenhang mit den fertilen Phasen. Die Weibchen waren über die gesamte Paarungszeit sexuell aktiv und kopulierten auch in azyklischen und trächtigen Phasen. Die fertilen Phasen der Weibchen waren zufällig verteilt. Das Auftreten weiblicher Rezeptivität war jedoch signifikant mit dem Anteil anderer sich paarender Weibchen assoziiert. Dies stützt die mating-synchrony-hypothesis und bietet eine mögliche proximate Erklärung für das ausgeprägte, nicht reproduktive Sexualverhalten bei dieser und vermutlich auch bei anderen Arten. Im Gegensatz zu zahlreichen Primatenarten, konzentrierten die Weibchen Vaterschaften nicht in hochrangige Männchen, sondern zeigten Paarungspräferenzen für Männchen unterschiedlichsten Ranges. Trotz ausgeprägter Promiskuität, paarten sich Weibche n wiederholt mit ihrem jeweiligen primären Partner . Die Ergebnisse meiner Studie haben insgesamt gezeigt, dass Assammakaken-Weibchen ihr Sexualverhalten adaptieren und von strikter hormoneller Kontrolle lösen. Dadurch können Weibchen den Paarungs- und Reproduktionserfolg der Männchen zu einem großen Teil manipulieren und kontrollieren. Diese Dissertation hat (1) erste Informationen über Reproduktionsparameter und life-history Merkmale bei dieser saisonalen und kaum erforschten Makaken-Spezies geliefert, (2) den wachsenden Wissensstand über Reproduktionsstrategien weiblicher Wirbeltiere erweitert, (3) neues Licht auf die Plastizität weiblicher Sexualität geworfen, und (4) zu einer Verfeinerung unseres Konzepts von intersexuellem Konflikt bezüglich Vaterschaft bei Primaten beigetragen.Sexual conflict is a prominent feature of animals living in multimale-multifemale groups, and drives the evolution of sex-specific reproductive strategies. Owing to divergent reproductive optima, males should compete to monopolize and mate with as many females as possible, whereas females should be more selective of their mates, leading to a coevolutionary arms race between the sexes. Facing the risk of infanticide by males, a source of intense sexual conflict, female primates have evolved counterstrategies and mechanisms to decrease male monopolization potential (i.e. male mating skew) and to manipulate male paternity estimates to overcome the female dilemma , i.e. to balance paternity concentration and dilution. The aim of this thesis was to investigate female reproductive strategies and underlying proximate mechanisms and constraints in a primate with low male contest competition, the Assamese macaque (Macaca assamensis). By combining demographic, behavioral and hormone data, I investigated general female reproductive parameters and life-history traits, and in addition, I visually monitored anogenital sexual swellings in order to investigate their functional significance. I examined female sexual activity and male consortships in relation to fertility, and investigated patterns of reproductive synchrony. I proposed and tested the hypothesis that females behaviorally coordinate their mating activity, and investigated also ovarian cycle synchrony. The study was conducted at Phu Khieo Wildlife Sanctuary in northeastern Thailand during two consecutive mating seasons (07/08 and 08/09). I collected focal animal (>800 hours) and ad libitum data from 16 Assamese macaque females living in a wild, fully habituated group consisting of 50-60 individuals. Furthermore, I collected more than 2300 fecal samples in order to describe ovarian cycle and pregnancy characteristics and to assess the timing of ovulations and conceptions using enzyme immuneassays (EIA) for estrogen, progestogen and androgen metabolites. Endo crine profiles revealed that non-invasive monitoring of female reproductive state is feasible in Assamese macaques. Patterns of fecal androgen excretion during gestation may allow for early pregnancy detection and prenatal sex determination. Gestation length and interbirth interval fell into the range of closely related species. Females were anovulatory during the non-mating season and mostly conceived during their first ovulatory cycle within the 4-month mating season, with 65% of conceptions confined to December and January. The small subcaudal sexual swellings did not signal ovulation probability, and females lacked copulation calls and signs of behavioral estrus all of which indicate that fertility is undisclosed to males in this species. Accordingly, the long sexual consortships by high-ranking males were not linked to female fertile phases. Females exhibited extreme extended sexuality and mated throughout the mating season including acyclic and pregnant stages. Female fertile phases were randomly distributed, but the occurrence of a female s receptivity was significantly associated with the proportion of other females mating on a given day, offering a potential proximate explanation for the patterning and maintenance of extended sexuality in this and presumably other species. In addition, and in contrast to numerous non-human primate species, females did not concentrate paternities to high-ranking males but expressed non-dominance based mating biases, i.e. they mated repeatedly with a primary partner despite exhibiting high rates of promiscuity. Overall, these results suggest that in response to constraints of reproductive and life-history traits, female Assamese macaques modify and emancipate their sexual behavior from hormonal control, and thereby manipulate and control largely mating and reproductive outcome. In conclusion, this PhD-project not only gathered initial information on reproductive parameters and life-history traits for the seasonally breeding and rarely studied Assamese macaque but also contributes to the growing body of knowledge that endeavors to understand reproductive strategies of female vertebrates, sheds new light on the plasticity of female sexual behavior, and contributes to a refinement of our concept of intersexual conflict over paternity in primates

Concealed fertility and extended female sexuality in a non-human primate (Macaca assamensis).

In numerous primates living in mixed-sex groups, females display probabilistic cues of fertility to simultaneously concentrate paternity to dominant males while diluting it amongst others as a means to reduce the risk of infanticide and to increase male care for offspring. A few species, however, lack these cues and potentially conceal fertility from males; yet, to date, little is known about mating patterns and their underlying proximate mechanisms in such species. Here, we investigated mating activity and sexual consortships relative to female reproductive state in wild Assamese macaques (Macaca assamensis), a species where females lack prominent anogenital swellings and copulation calls. During two mating seasons (2837 contact hours) we recorded sexual and social behaviors, sexual consortships, and collected 1178 fecal samples (n = 15 females) which were analyzed for progestogen concentrations to assess female reproductive state and to determine the timing of ovulation and conception. Although mostly conceiving in their first ovarian cycle, females were sexually receptive throughout the entire 4-month mating season, and within-cycle mating frequencies were not increased during fertile phases. Dominant males did not monopolize fertile matings, and consortships by high-ranking males lasted for long periods, which were not exclusively linked to female fertile phases. Furthermore, females copulated promiscuously but not randomly, i.e. for almost every female, matings were concentrated to a certain male, irrespective of male rank. Collectively, we demonstrate that fertility is undisclosed to males. The extreme extended female sexuality facilitated by concealed fertility may allow females to create differentiated mating relationships within a promiscuous mating system. Our study provides important new insight into the plasticity of female sexuality in non-human primates