Grooming distributions between anoestrous and oestrous females

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Chapter 3  Grooming distributions between anoestrous and oestrous females

Abstract

It has been suggested that allogrooming among primates is a strategy for enhancing reproductive success, either by allowing males to enhance their proximity to oestrous females, or by influencing female choice through the development of affiliative relationships with males. Female chimpanzees have obvious swollen anogenital regions at or close to ovulation, which males could recognise as signalling receptivity and therefore, by adapting their grooming investment accordingly, males could increase their copulatory success. Swollen females may also increase grooming interactions with males so as to keep preferred males close by during a period characterised by considerable harassment from other males, and thereby obtain protection and increase the likelihood of copulation with preferred partners. Five and a half years of grooming data from a group of free-living chimpanzees (Pan troglodytes) in the Budongo Forest, Uganda, were examined to investigate how sexual swellings influence grooming behaviour between males and females of different age classes. Based on the availability of oestrous females, Bonferroni confidence intervals revealed that anoestrous adult and subadult females gave and received significantly less grooming to and from adult males than expected, but that oestrous adult and subadult females gave and received significantly more grooming to and from adult males than expected. Adult (anoestrous and oestrous) females gave and received significantly less grooming to and from subadult males, whereas subadult females gave and received significantly more grooming to and from subadult males than expected. Wilcoxon rank sum tests revealed that oestrous adult females devoted more time to giving and receiving grooming to and from adult males than did anoestrous adult females. Oestrous subadult females gave both adult males and subadult males more grooming than did anoestrous subadult females. Grooming interactions between adult males and oestrous adult females were initiated significantly more often by males, but those between anoestrous subadult females and adult males were initiated significantly more frequently by females. Grooming interactions between adult males and oestrous adult females were more likely to be terminated by males. Both age and oestrous swellings influence grooming interactions between chimpanzees, and grooming may be a strategy used by males to increase their access to copulation opportunities, whereas females may use grooming to increase protection from harassment during swollen periods and the likelihood of copulation with preferred partners.
Keywords: Chimpanzees, Pan troglodytes, grooming, oestrous, Budongo Forest
Running Title: The influence of oestrous swellings on the grooming behaviour of chimpanzees of the Budongo Forest, Uganda

Introduction

One of the main objectives of primate socio-biology is to generate a greater understanding of the variations observed in social behaviour and how they tie in with biological function. One of the most frequently observed social behaviours in primates is allogrooming, (one individual grooms another) indicating willingness to invest time and effort in relationships with other group members (Walters and Seyfarth 1987; Dunbar 1992; Hemelrijk and Lutjein 1998), which may be essential for the development of cooperative relationships (Van Hoof and Van Schaik 1994) and used to establish and reinforce social relationships between group members (Walters and Seyfarth 1987). Grooming helps to remove ectoparasites and other debris from an individuals coat (Poirier 1970; Tanaka and Takefushi 1993) whilst also stimulating the productions of endorphins (Keverne et al. 1989). Seyfarth (1980) suggested that allogrooming occurs more frequently than is necessary for hygienic purposes alone and therefore, probably has social significance. Support for this suggestion of social reinforcement through grooming interactions between group members comes from demonstrations of grooming reciprocity (chimpanzees: Hemelrijk and Ek 1991; Watts 2000; vervet monkeys: Hemelrijk 1990), preference of allies to groom each other (tufted capuchins: Di Bitetti 1997), gaining of social acceptance by group members (Poirier 1970), tolerance at feeding sites (Barton and Whiten 1993), support during conflicts (Seyfarth 1976; Hemelrijk 1990), access to new born infants (Seyfarth 1976; Altmann 1980; Henzi and Barrett 2002) and sharing of food (De Waal 1989, 1997).
An additional suggestion is that grooming may be used by individuals to increase reproductive success (Weingrill 2000). By using grooming to strengthen social bonds, chances of copulations may also be increased (Michael et al. 1978; Tutin 1979). It may 64 consequently be in a male’s best interest to invest time and effort in grooming potentially reproductive females rather than non-reproductive ones, whereas females may benefit more by developing grooming relationships with strong healthy adult males rather than generally smaller, weaker subadult males. (Anderson and Bierlet 1994)
Males may be able to recognize that females are sexually receptive, through visual cues such as anatomical changes during the periovulatory period (Hamilton 1984; Anderson and Bielert 1994). As females progress through their reproductive cycles, changes in oestrogen and progesterone levels cause swelling of the female’s anogenital region (e.g., chimpanzees and baboons). Males would benefit if they were able to use these visual cues to assess a female’s sexual receptivity and invest his grooming investment accordingly.
Between 26 and 35 species of primates are known to have sexual swellings (Clutton-Brock and Harvey 1976; Hrdy and Whitten 1987; Anderson and Bielert 1994) but none of these are prosimians or new world monkeys (Dixson 1983). Within the Old world species that do have sexual swellings, they occur mainly in species that have a multimale social organization (Clutton-Brock and Harvey 1976) such as red colobus monkeys Colobus bodius, macaques, baboons, mangabeys Cercocebus spp and chimpanzees.
Suggestions as to why sexual swellings have only evolved in some species include: Being used as a ‘passport’ by young females to safely join new groups (Nishida 1979; Pusey 1979; Moore 1984; Wallis and Goodall 1993; Boesch and Boesch-Achermann 2000); strategies used by females to compete with each other for access to mating opportunities with preferred males (Pagel 1994) although experimental data do not support this idea (Radwan 1995; Wiley and Poston 1996); initiating competition between males and females to help determine male quality (Clutton-Brock and Harvey 1976); the many-male hypothesis (Hrdy 1981; Hrdy and Whitten 1987), suggesting that females mate with a number of males, resulting in positive interactions between males and offspring thereby suggesting an illusion of paternity and decreasing the chances of infanticide (Goodall et al. 1979; Hrdy 1979; Taub 1980; Harcourt 1981; Hrdy 1981; Zinner and Deschner 2000) and serve as accurate ovulation indicators (Hamilton 1984) due to positive associations between females with swollen swellings and sexual behaviour having been observed in many species displaying this phenomenon (Rowell 1972; Wallis 1982; Dixson 1983).
If grooming is one of the strategies that males use to increase their chances of copulation, grooming with females would be expected to increase during female oestrous periods as has been found in captive chimpanzees (Wallis 1992). Observations suggest that this may also occur in free-living chimpanzees, but this has not been empirically investigated (Goodall 1986). Swollen females may also increase grooming interactions with specific males to keep preferred males close by during a period sometimes characterised by considerable harassment from other males. Females thus obtain protection as well as increase the likelihood of impregnation by a preferred partner (Smuts and Smuts 1993; Stumpf and Boesch 2005). Assuming both males and females benefit from increased grooming during female receptive periods, the effort put into initiating and maintaining grooming bouts by the different sexes may also change. Furthermore, if grooming is used as a strategy to increase reproductive success, the age class of an individual would be expected to have an impact on these grooming relationships.
Chimpanzees exhibit both extensive social grooming and obvious sexual swellings. The menstrual cycle of female chimpanzees is ~ 36 days (Young and Yerkes 1943) and is characterised by changes in the size, shape and colouring of the anogenital region (Wallis 1992). The initial swelling lasts an average of 7.6 days (Young and Yerkes 1943), and maximum swelling for up to 17 days (mean 10-12) (McGinnis 1979), with ovulation taking place during the last one or two days (Graham 1982). The following four days results in a rapid decrease in the size of the swelling (Wallis 1982) and then for the next 14 days the anogenital area remains flat (McGinnis 1979). Females may also experience these swellings during the early stages of pregnancy and it is suggested (Wallis 1982) that any benefits gained by oestrous females will also apply to swollen pregnant females. Females tend to transfer to new communities whilst displaying anogenital swellings, and therefore being swollen whilst pregnant will create an illusion of sexual receptivity and facilitate the increase of genetic diversity between communities.
Adolescent or subadult females also display sexual swellings but may go through approximately 19 menstrual cycles before becoming fertile (Tutin 1980; Boesch and Boesch-Achermann 2000), which has been suggested as a strategy to allow practice of sexual behaviour to ensure insemination with no delay once they become fertile (Short 1976; Turke 1984; Kalkstein 1991). Adult males of many species show an aversion to mating with subadult females (Strum and Western 1982; Smuts 1985; Van Noordwijk 1985; Anderson 1986), so it would be expected that if grooming is used as a strategy to increase copulations, adult males would show a similar aversion to grooming subadult females. Subadult males on the other hand may be physiologically capable of inseminating females, but are generally smaller, weaker, have shorter canines and are subordinate to adult males and therefore less effective at protecting females and infants (Anderson and Bierlet 1994) and therefore should be the less preferred grooming age of sexually receptive adult females.
The aim of this chapter is to describe the relationship between sexual swellings and grooming behaviour between males and females of different age classes within a group of free-living chimpanzees. The main research question that will be addressed in this chapter is: How does the presence of sexual swellings influence grooming interactions between males and females of different age classes? Taking into account the number of females present at any one time during the study period and whether they had either no swelling or swelling, It is hypothesised that:

  1. If males are the instigators for reproductive advantages then it would be expected that males give more grooming to females during this time;
  2. If females are using grooming of preferred males to protect themselves then it would be expected that more grooming by females to adult males would occur.
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Following these it was predicted that:

  1. Oestrous females give and receive more grooming bouts to and from males than do anoestrous females
  2. Oestrous females allocate more of their grooming time to males than anoestrous females
  3. The oestrous  state  of  a  female  influences  which  sex  initiates  a  grooming interaction, with males initiating more often with oestrous than anoestrous females
  4. The oestrous state of a female influences which sex terminates a grooming interaction, with males terminating less often with oestrous than with anoestrous females

Study area and methods

Study area

The Budongo Forest Reserve is made up of 793 km² of moist semi-deciduous forest and grassland, and is situated at a mean altitude of 1100m on the edge of the western Rift Valley in western Uganda (Eggeling 1947; Plumptre 1996). The average annual rainfall of the region is approximately 1400 mm, with a dry season between December and February. Daily mean temperatures range between 14ºC and 28ºC (Eggeling 1947).
The Sonso region (1º44′ N, 31º33 E’) in which this study was carried out lies well within the forest and is named after the river flowing through the area. Although most of the forest was selectively logged in the past, the logging industry halted operations within the study area between 1947 and 1952 (Plumptre 1996). This, together with forest dynamics, has resulted in the Sonso region of the forest being made up of various forest types, including mixed forest, colonizing forest, swamp forest and ironwood forest (Eggeling 1947; Reynolds 1992). The study site was established in 1990 and is maintained by the Budongo Forest Project (Reynolds 1992; Plumptre et al. 1997). A system of trails covering an area of approximately 31km² aids travel through the study area, allowing researchers relatively easy access to the forest.

Study group

Between 1990 and 1994 with the effort of Nick Newton-Fisher and field assistants Geresomu Muhumuza and Zephyr T. Kiwede the chimpanzees were followed and  eventually allowed observers to follow them at close quarters throughout the day. Individual chimpanzees of the Sonso group have subsequently been habituated, sexed and identified, and have all been given a two-letter identification code. The chimpanzees spend most of their time within an area of about 7km² with each individual having its own ‘core’ area (Newton-Fisher 2000).
During the period of this study, the Sonso group consisted of between 36 and 54 individuals (Table 3.1). Eleven of the Sonso chimpanzees had injured limbs as a result of being caught in snares, set by the local people to catch duiker and forest pigs (Waller and Reynolds 2001). Four other groups of chimpanzees are known to occur within the forest, two (Busingiro and Kaniyo-Pabidi groups) of which are currently being habituated for tourism purposes. The other two groups (The Nature Reserve and Waisoke groups) have not yet been habituated or studied but both share boundaries with the study group.

Data collection

Data were collected continuously between September 1995 and April 2001 as part of a long-term study on the behaviour and ecology of the Sonso chimpanzees. Eleven field assistants (a mean of four at any given time) employed by the Budongo Forest Project conducted sampling, daily (weather permitting) between 07:30 and 13:00 and then again between 14:00 and 16:00 on an ad libitum basis (Altmann 1974) whilst following the chimpanzees. Each sample recorded the identities of individuals present, interactions between individuals (grooming, playing, aggression, copulations etc) initiators and terminators of interactions, duration of interactions (recorded to nearest minute) and female anogenital swellings. Subadult and adult females were allocated a score depending on the size of their sexual swelling. The following scores were allocated by observers: 0 – no swelling, 1 – ¼ swelling, 2 – ½ swelling, 3 – ¾ swelling and 4 – full swelling. The following abbreviations will be used throughout the remainder of the chapter to refer to different age-sex classes: AM – adult males, AF – adult females, SM – subadult males and SF – subadult females.

Summary
Acknowledgments 
Disclaimer and constraints to this dissertation
Contents
List of Tables
List of Figure
Chapter 1: General Introduction
1.1 Relevance of study
1.2 Key questions and dissertation outline
1.3 References
Chapter 2: Grooming distributions across age-sex classes
2.1 Introduction
2.2 Study area and methods
2.2.1 Study area
2.2.2 Study group
2.2.3 Data Collection
2.2.4 Analysis
2.3 Results
2.3.1 General grooming distributions between age-sex classes
2.3.2 Mutual versus unidirectional grooming bouts
2.3.3 Grooming distributions of different age-sex classes
2.3.4 Number of grooming partners
2.3.5 Grooming reciprocity between age-sex classes
2.4 Discussion
2.5 References
Chapter 3: Grooming distributions between anoestrous and oestrous females
3.1 Introduction
3.2 Study area and methods
3.3 Results
3.4 Discussion
3.5 References
Chapter 4: Grooming distributions and copulations
4.1 Introduction
4.2 Study area and methods
4.3 Results
4.4 Discussion
4.5 References
Chapter 5: A comparative analysis of using scan-focal versus ad libitum sampling methods in the investigation of grooming behaviour 
5.1 Introduction
5.2 Study area and methods
5.3 Results
5.4 Discussion
5.5 References
Chapter 6: Synopsis and conclusion 
6.1 References
APPENDIX 
GLOSSARY
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