Female Mate Preferences Among Pan troglodytesschweinfurthii of Kanyawara, Kibale NationalPark, Uganda

Katharin Pieta

Received: 16 February 2007 /Accepted: 10 March 2008 /Published online: 22 July 2008# Springer Science + Business Media, LLC 2008

Abstract Studies of reproduction among chimpanzees traditionally have focused onthe mating strategies of males. However, less is known about the mating strategies offemale chimpanzees and whether they demonstrate mate choice. I investigatedsexual behavior and female mate preference in the chimpanzees of the Kanyawaracommunity. To estimate mate preferences, I analyzed female proceptivity andresistance rates of 6 estrous females toward a total of 13 males as well as malesolicitation and aggression rates toward females. Males solicited some females moreoften than others for mating and preferred them throughout estrus, not only duringthe periovulatory period (POP), when conception was most likely. In contrast,though females had strong mate preferences in both non-POP and POP, their matepreferences were not consistent between the 2 phases. The shift in mate preferencesis evidence of a promiscuous yet tactical mating strategy to confuse paternity.Further, females were more proceptive and generally less resistant toward eschewedmales in non-POP and more proceptive and less resistant toward preferred males inPOP. Hence, the results indicate that females attempted to mate selectively duringthe fertile phase. Kanyawara female chimpanzees appear to change their matingstrategies and selectivity during estrus and thus may pursue a mixed reproductivestrategy. The tactic may allow females to deceive males, indicating that promiscuityamong chimpanzee females may be more strategic than previously thought.

Keywords chimpanzees . female mate preference . Pan troglodytes schweinfurthii .

reproductive strategies . sexual behavior

Int J Primatol (2008) 29:845–864DOI 10.1007/s10764-008-9282-5

K. Pieta (*)Department of Anthropology, University of Vienna, A-1091 Vienna, Austriae-mail: katharin_pieta@yahoo.com

Introduction

Apes are characterized by a variety of social systems including monogamous pairs,1-male polygynous groups, and multimale multifemale groups of various sizes and sexratios (Kappeler and van Schaik 2002; Terborgh and Janson 1986; Wrangham 1987).They are thus valuable as testing models of reproductive strategies, a crucial elementin their life-histories. Long-term studies on apes offer a wealth of data that is otherwiseoften difficult to obtain and provide new insights into female reproductive strategies ofour closest living relatives. Emerging research on wild female chimpanzees has shownthat factors such as dominance rank (Pusey et al. 1997), home range (Williams et al.2004), and body mass (Pusey et al. 2005) affect reproductive success. Wrangham(1997) stated that even where females interact rarely or subtly, female initiative can bea major force in the evolution of social systems, and that covert behavior by femalechimpanzees may also be important in the sexual realm. Thus, examining female matechoice is expected to reveal novel information on mating strategies in the species.Hasegawa and Hiraiwa-Hasegawa (1983), Takasaki (1985), and Tutin (1979)described 3 distinct mating patterns for chimpanzees: 1) Opportunistic mating: Thefemale mates with many or all available males in the group. Males may or may notcompete for mating access. 2) Possessive mating (mate guarding): One, mostly high-ranking male forms a short-term relationship with an estrous female and monopolizesher for exclusive mating access and therefore prevents lower-ranking males in thegroup from copulating with her. In Kibale National Park, Ngogo, the largest habituatedstudy group, Watts (1998) described coalitionary mate guarding by 2 or 3 males. 3)Consortship: One male leads an estrous female away from the group and has exclusivemating access. The pair travels together for a few hours, days, or even weeks. Tutin(1979) argued that the existence of nonpromiscuous mating patterns is important,because sexual selection can operate only under restrictive patterns, wherein certainmales can increase their reproductive success at the expense of others via femalechoice, male-male competition, or both. Consortships with cooperative females aremore successful and therefore mediated by female choice, while the possessive matingpattern is considered to be the outcome of male mate choice (Hauser 1989; Tutin1979, 1980).

The occurrence of mate choice in the opportunistic mating pattern is less clear.According to sexual selection theory, females should mate selectively with high-quality males to enhance maximal reproductive success (Anderson 1994; Darwin1871). However, promiscuous mating in female chimpanzees does not accord withthe view of females being the choosy sex. Several studies on a variety of specieshave shown that despite the costs, females that copulate with multiple males arereproductively more successful than females with only 1 partner (Birkhead 2000).Some suggested benefits of promiscuity are confusing paternity and avoidinginfanticide (Hrdy 1979; van Noordwijk and van Schaik 2000; van Schaik et al.2000), enhancing high-quality genes through male-male and sperm competition(Clutton-Brock and Harvey 1976; Edvardsson et al. 2007), and increasing theprobability of fertilization (Burley 1989; Small 1990). Costs of promiscuity areenergy and time (Beach 1976; Matsumoto-Oda and Oda 1998; Wrangham 1979),female-female competition (Matsumoto-Oda et al. 2007), and male sexual coercion(Muller et al. 2007; Smuts and Smuts 1993).

846 K. Pieta

Female chimpanzees live in a male-bonded and male-dominating society andreceive various amounts of aggression from males, depending on their age andfecundity (Goodall 1986; Matsumoto-Oda and Oda 1998; Muller and Wrangham2004). Thus, male sexual coercion might obscure female mate preferences. Femalemating behavior could therefore be influenced by male aggression either in terms ofpast aggression received or anticipated in the future (Stumpf and Boesch 2005).Further, the sexes vary in their ecological and physiological constraints. Femalesinvest more into their offspring than males do. The higher parental effort requireslong interbirth intervals and higher energy demand, and therefore food is the majorconstraint of reproductive success for females. In contrast, the limiting resource ofreproductive success for males is mating access to estrous females (Emlen and Oring1977; Trivers 1972; Wrangham 1980). Accordingly, one expects females and malesto exhibit conflicting mating strategies, and hence, mate preference. In view of theconflicting interests of the sexes it is necessary to distinguish female matepreferences from male mate preferences (cf. Muller et al. 2006, 2007; Stumpf andBoesch 2005).

Because chimpanzee populations differ in their behavioral and cultural repertoire(Boesch et al. 2002; Whiten et al. 1999), examining sexual behavior and choices ofmates in various field sites with different social and ecological constraints mightenhance our knowledge of the diversity and similarities in the species. Studies onfemale mate choice in wild chimpanzees existed only for West African chimpanzees(Pan troglodytes verus) in the Taï National Park, Côte d’Ivoire (Stumpf and Boesch2005, 2006), and East African chimpanzees (Pan troglodytes schweinfurthii) inGombe (Tutin 1979) and Mahale (Matsumoto-Oda 1999), Tanzania. I examined dataon female mate preference in the Kanyawara chimpanzee community, in KibaleNational Park, Uganda. I use the term female mate preference to define the male afemale would have liked to mate with, i.e., proceptive behavior before a possiblecopulation. Accordingly, female mate choice is the implementation of thatpreference, i.e., copulation after female proceptive behavior; no copulation afterfemale resistance behavior (Halliday 1983). I obtained all data in an opportunisticmating setting. Though males may have competed with each other over matingaccess and may have tried to be possessive toward the estrous female, they were notable to monopolize her. Data on male sexual invitations and male aggression towardfemales served to control for potential male influence on female behavior. Iaddressed 2 questions: 1) Do female chimpanzees prefer particular males? 2) Dofemale chimpanzees exhibit different preferences during the fertile vs. nonfertileestrous period?

Methods

Study Site and Subjects

The chimpanzees were members of the Kanyawara community in Kibale NationalPark, western Uganda (0°34′N and 30°21′E). The study area covers primary forest,logged areas with regenerating forest, grassland, swamp, and agriculture (Chapmanand Wrangham 1993; Struhsaker 1975). Isabirye-Basuta (1989) studied the

Female Mate Preferences of Pan troglodytes schweinfurthii 847

chimpanzees of Kanyawara systematically for the first time in the early 1980s,followed by Richard Wrangham, who established the Kibale Chimpanzee Project inSeptember 1987 and has continued studies to the present. No one has provisionedthe chimpanzees.

At the beginning of the study, the Kanyawara community comprised 53 individuals:16 parous females, 10 adult males, 3 nulliparous females, 3 subadult males, 10 juveniles,and 11 infants. Five infants were born in the course of the study. One female, NL,became parous in February 2000. One male, KK, reached adult age, 16 yr, in July 2001(Goodall 1983). Two adult males (SY, last seen in July 2000 and LB, last seen inFebruary 2001) and 2 adult females with their dependent infants (KL, last seen inDecember 2000 and JO, last seen in March 2001) disappeared during the study.

Data collection

Focal Subjects I followed chimpanzees from early morning when they awoke intheir night nests until the evening, when they constructed their night nests. Icollected a total of 330 observation hours between May 1999 and December 2001via continuous focal sampling (Altmann 1974) following 6 estrous females. Iconducted pregnancy tests with human pregnancy test kits (Craig Medical, Vista,CA; Quidel, San Diego, CA). Of 3 parous females (JO, OU, and TG), 2 conceivedduring the study (TG: end of March 2000, OU: August 2000; Emery Thompson,pers. comm.). JO died of a respiratory disease in March 2001 before she was able tobecome pregnant. Because parous females have higher probabilities of conceptionthan those of nulliparous females (Wrangham 2002), I refer to the parous femalesJO, OU, and TG as high-fecund females, i.e., high probability of conception. BR andLR were both nulliparous females born within the Kanyawara community. BR waslast seen in August 2000 and thereafter presumably transferred to a neighboringcommunity. LR conceived her first offspring in December 2002, 1 yr after my studyhad ended. LR is the first female of the Kanyawara chimpanzee community thatbirthed within her natal group and did not emigrate (Wrangham, pers. comm.). NLwas a parous female that resumed cycling in August 2000, only 6 mo after birthingher first offspring. NL conceived her second offspring in September 2003 (EmeryThompson, pers. comm.), 21 mo after I completed my observations. Thus, NL’spostpartum swellings were nonconceptive during my study. Because NL had a longtime period of nonconception cycles, I refer to her and nulliparous females BR andLR as low-fecund females, i.e., low probability of conception. The 6 females and alladult and subadult males of the study including their estimated ages fromobservations by Isabirye-Basuta and Wrangham (Wrangham, pers. comm.), are inTable I. The 13 males are in descending order of their rank with MS as the α-male. Iused the adjusted yearly dominance rank of 2000 (Muller, pers. comm.), the year thatOU and TG conceived. The estimated ages in Table I refer to the same year.

Sexual Swellings I used a simple 3-point scale to record the degree of tumescenceof the sexual swelling for each female: 1=no swelling, 2=partial swelling, and3=maximal swelling (Furuichi 1987; Wallis 1992). I analyzed data only onmaximally swollen females. Though both females continued cycling after conception(number of cycles with full swellings after conception: OU: 1 cycle, TG: 4 cycles;

848 K. Pieta

Emery Thompson, pers. comm.), I analyzed only data of females when they were notpregnant because it is biologically more meaningful. From the evolutionary point ofview, copulations that result in pregnancies are more relevant. For the same reason, Iclassified the data into periovulatory period (POP) and non-periovulatory period(non-POP). When the classification was not possible (error±1 d), I eliminated thedata from analysis. Based on the results for captive chimpanzees (Graham 1981),former students of reproduction strategies of wild chimpanzees assumed thatovulation takes place on the last day of maximum tumescence (Hasegawa andHiraiwa-Hasegawa 1983; Matsumoto-Oda 1999; Tutin and McGinnis 1981). A morerecent study on wild West African chimpanzees showed more variability of timing ofovulation. According to Deschner et al. (2003), if cycles were adjusted to the lastday of maximum tumescence and the day was taken as d 0, probability of fertilitywas highest between d –2 and –5. Thus if endocrine markers for determiningovulation are not feasible, one should use an earlier window to indicate theperiovulatory period than previously assumed. This is in accordance with data oncomposite cycle profiles on wild East African chimpanzees for Kanyawara,Budongo, and Gombe (Emery Thompson 2005). I therefore classified POP usingd –2 to –5. The total numbers of cycles obtained for each female are in Table I, aswell as the number of non-POP and POP. Because I could not obtain observationsfor both non-POP and POP for each cycle, the numbers vary between the 2 periods.

Table I All females and males included in the study

Individual Age Parity Number of cycles

Total Non-POP POPFemalesJosta (JO) est. 40 Parous 4 3 3Outamba (OU)* est. 21 Parous 2 2 2Tongo (TG)* est. 20 Parous 1 1 1Nile (NL) est. 18 Parous; postpartum 4 3 4Barbara (BR) est. 11 Nulliparous 6 5 2Rosa (LR) 11 Nulliparous 10 10 4MalesImoso (MS) est. 21Big Brown (BB) est. 34Light Brown (LB) est. 32Tofu (TU) est. 40Johnny (AJ) est. 26Slim (SL) est. 29Yogi (YB) est. 27Stout (ST) est. 45Stocky (SY) est. 36Makoku (LK) est. 18Kakama (KK) 15Twig (PG) 12Eduard (ED) 12

Females: high-fecund females (regular), low-fecund females (italic), conception during observation period(*). Total number of estrous cycles may vary between POP (periovulatory period) and non-POP owing tolack of observations for either period of some cycles. Males: adult (regular), subadult (italic). KK turned toadulthood during the study period (July 2001). Males are listed in descending order of their rank with MSas α-male (adjusted yearly dominance rank of 2000, the year that OU and TG conceived). Age: estimatedat year 2000.

Female Mate Preferences of Pan troglodytes schweinfurthii 849

Behavior I recorded all behavior of the focal subjects via all-occurrence sampling,with the main focus on sexual behavior. Detailed descriptions of chimpanzeebehavior are in Tutin and McGrew (1973), Goodall (1986), and Nishida et al.(1999). I limited the scope of this article to analysis of the initiation and resistance ofsexual behavior and to male aggression toward females. In chimpanzees, either themale or the female can initiate sexual activity. Male solicitation behavior is anymale-initiated sexual behavior, e.g., approaching, glancing, gazing, branch-shaking,and male inviting position. Female primates exert direct mate choice via responses toopportunities to copulate, i.e., initiating or refusing sex (Smuts 1987).

I evaluated female mate preference via quantifying proceptivity and receptivity,i.e., female solicitation and female resistance to male solicitations (cf. vervets: Keddy1986; ring-tailed lemurs: Pereira and Weiss 1991; chimpanzees: Stumpf and Boesch2005). Female proceptivity is female-initiated sexual behavior, i.e., a femaleapproaching a male and presenting for copulation without preceding male-initiatedsexual behavior. Receptivity is the responsiveness of females to cues provided bymales (Beach 1976). Female chimpanzees can either cooperate or resist a solicitingmale. A cooperating female chimpanzee approaches the soliciting male and presentsfor copulation (Tutin 1979). Female resistance is defined as the resisting response,i.e., ignoring, avoiding, screaming or leaving, toward a soliciting male. Femaleresistance indicates only the female’s initial response to a male’s solicitation and notwhether the solicitation leads to copulation.

Male chimpanzees may influence female behavior via coercion, which mayconsequently obscure the expression of female mate preferences. Hence, I recordedall male aggressive behaviors toward a female in addition to male solicitation as away to control for the conditions.

I recorded party composition (presence in the party) every 15 min to calculate thedyadic association time per female-male dyad.

Data Analysis

Descriptive Analysis I express all rates of behavior —excluding resistance— ascounts per hour for each female-male dyad. To assess female mate preferences, Iused 2 measures and calculated rates of female proceptivity and resistance (Stumpfand Boesch 2005). 1) Proceptivity rates are the total number of unsolicitedpresentations by a female to a male divided by the dyadic association time duringestrus. If a male never associated with a certain female, I could not calculate theproceptivity rate for that female-male dyad and it is a missing value. 2) Resistancerates are the total number of female resistance events divided by the number of malesolicitations for each female-male dyad. If a male never solicited a certain female, Icould not calculate the resistance rate for that female-male dyad, i.e., the cell is 0/0and therefore a missing value. With the 2 measures, I could classify individual malesfor each female, i.e., female-male dyads, into 1 of the 3 categories: preferred, neutral,and eschewed. To begin with, I calculated for each female the average proceptivityrate (and resistance rate) of all males, i.e., each female had a mean value ofproceptivity rate, and resistance rate, respectively. Subsequently, I classified a maleas preferred by a female when the female proceptivity rate, or resistance rate, towardthe male deviated >25% above or below her average proceptivity or resistance for all

850 K. Pieta

males. Conversely, I classified a male as eschewed, i.e., nonpreferred, by a femalewhen her proceptivity rate or resistance rate toward him deviated >25% below orabove her average proceptivity or resistance for all males. When the proceptivity orresistance rate was between the 25% margin, I classified the male as neutral. The25% mark is arbitrary but appears to be sufficiently high to detect differences in afemale’s behavior toward different males (Stumpf and Boesch 2005). Each femalecould prefer or eschew >1 male (Table II).

To test whether the behavior of males influenced the behavior of females, Icalculated rates of male solicitation and male aggression toward females. Malesolicitation rates are the total number of solicitations by a male toward a femaledivided by the dyadic association time during estrus. Male aggression rates are the

Table II Female mating preferences for individual males based on proceptivity or resistance rates duringestrus

Preferred Neutral Eschewed

Non-POP

Proceptivity JO MS TU AJ BB LB SL YB ST SY LK KKPG ED

OU MS AJ YB ST LKKK

SL BB LB TU SY PG ED

TG AJ ED MS BB TU YB LKKK

ST PG

NL MS AJ LK KK ED SL LB TU YB ST PGBR SY LK PG ED MS BB LB TU AJ SL YB ST

KKLR TU YB KK LB PG MS BB AJ SL ST LK ED

Resistance JO LB TU AJ SL YB ST MS SYOU BB LB TU AJ YB ST

LKKK MS SL PG ED

TG MS BB TU AJ YB ST LK KK PG EDNL SL ST LK KK ED MS LB AJBR SL KK PG ED MS LB AJ YB LKLR MS BB TU AJ KK

EDST PG SL YB LK

POP Proceptivity JO MS LB TU SL YB ST BB AJ SY LK KK PG EDOU MS BB ST LK LB TU AJ SL YB SY KK PG

EDTG MS AJ LK BB TU YB ST PG EDNL LB LK ED YB MS BB TU AJ SL ST KK PGBR AJ LK PG MS BB LB TU SL YB ST SY

KK EDLR LB ST KK ED SL MS BB AJ YB LK PG

Resistance JO LB TU SL YB ST SY MS BBOU TU AJ ST LK KK MS LB YB PGTG YB ST MS TU AJ BBNL BB LB TU AJ ST PG MS LK SL KK EDBR TU SL ST KK PG

EDMS BB LB LK

LR BB LB KK PG YB LK MS AJ SL ST

Females: bold font. Males: plain font. POP: periovulatory period. Categories: Preferred: femaleproceptivity rate (or resistance rate) toward a male deviated >25% above (or below) the female’s averageproceptivity (or resistance) for all males. Eschewed: proceptivity rate (or resistance rate) toward a maledeviated >25% below (or above) the female’s average proceptivity (or resistance) for all males. Neutral:proceptivity or resistance rate was in between the 25% margin.

Female Mate Preferences of Pan troglodytes schweinfurthii 851

total number of aggressive behaviors, e.g., chases, charges, contact aggression, of amale toward a female divided by the dyadic association time during estrus. From thefemale point of view, they are rates of received aggression. Because a female’sbehavior has more evolutionary consequences during her fertile vs. her nonfertileperiod, I calculated all rates of behavior for non-POP and POP.

Statistical Analysis To assess if female proceptivity or resistance behavior wasunbiased toward males, i.e., neutral males, or if they biased their behavior towardindividual males, i.e., deviate from the average; preferred or eschewed males, Icompared the number of individuals in the neutral male category with the poolednumber of individuals in the preferred and eschewed male category via binomialtests for each female separately in non-POP and POP; e.g., for proceptivity rate innon-POP for JO, in total 13 males were in the preferred and eschewed male categoryand no male was in the neutral category (Table III). The probability parameter forboth groups —biased and unbiased— was 0.5. I obtained 6 p-values for each femalefor proceptivity or resistance in both non-POP and POP phases. To obtain an overallp-value, I again used binomial tests. The probability parameter for both groups —count of significant females and count of non-significant females— was 0.5. Forexample, for proceptivity rate in non-POP, I obtained for 5 females significantp-values and for 1 female a non-significant p-value; the binomial test for the values 5and 1 is not significant. Owing to the small sample size, only when 6 of 6 femalesshowed significant p-values was the overall p-value significant.

To compare female behavior across their estrous period on a group level, I createdrectangular matrices of proceptivity or resistance rates of non-POP and correlatedthem with the corresponding rates in POP. Because my investigations focused on thefemale point of view, I used the focal females as rows, i.e., 6 rows, and the 13 malesas columns. I used rowwise matrix correlations and Kr and Kendall’s tau (τrw)statistics to take individual variation into account (Table III; de Vries 1993;Hemelrijk 1990). Because I could not calculate all rates for all dyads, my socialmatrices had missing values (percentage of missing values per matrix: proceptivityrate, non-POP, 7.7%; POP, 9%; resistance rate, non-POP, 25.6%; POP, 30.8%. Foreach female, average missing values/range: JO, 2.5/0–5; OU, 1.25/0–4; TG, 4.25/3–

Table III Rowwise average Kendall's rank correlation coefficient (τrw) between rates of non-POP andPOP matrices

Female Proceptivity Female Resistance Male solicitation Male aggression

τrw p τrw p τrw p τrw P

Females 0.07 0.240 0.11 0.170 0.37 0.001 −0.03 0.393HF 0.12 0.215 0.22 0.094 0.52 0.001 0.14 0.199LF 0.03 0.430 0.01 0.48 0.23 0.041 −0.28 0.040

All probabilities represent the average of 15 correlations with imputations and are estimated based on2000 permutations.p: 1-tailed probability of the right tail of the permutation distribution (or of the left tail if τrw-value isnegative).Females: all focal females; HF: high-fecund females; LF: low-fecund females

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7; NL, 2.5/1–5; BR, 1.75/0–4; LR, 2/1–3). One cannot calculate rowwisecorrelations between 2 matrices that contain missing values via the permutationprocedure used to obtain p-values. Therefore I used a method of multiple imputationof multiple values (de Vries, pers. comm.). The first step is to fill in a randomnumber for each missing value in a temporary copy of the matrix. The randomnumber should lie within the range of the known values of all females, i.e.,proceptivity rate: between 0 and the highest possible rate; resistance rate: between 0and 1. The second step is to choose randomly a value from the set of non-missingvalues and the filled-in missing values from the temporary matrix, i.e., for eachfemale choose randomly from the 13 values now present in each row, to fill in themissing values in the real matrix. I performed the 2-step procedure of multipleimputation of multiple values 15 times per matrix, thus obtaining 15 matrices withimputed values for each initial matrix. Then I correlated the matrices I chose tocorrelate, e.g., first matrix of proceptivity rates in non-POP with first matrix ofproceptivity rates in POP, second matrix of proceptivity rates in non-POP withsecond matrix of proceptivity rates in POP, etc., and I calculated the 15 Kendall’s tauvalues (τrw), and the corresponding p-values with the standard permutationprocedure. Finally, I calculated a likely τrw-value by taking the average of the 15τrw-values and an estimate of the corresponding p-value that I obtained by taking theaverage of the 15 p-values. Fifteen imputed matrices were sufficient to obtain areliable estimate of the τrw-values and corresponding p-values (de Vries, pers.comm.). The higher the variation in τrw-values and corresponding p-values is, thehigher is the uncertainty and the more imputed matrices need to be generated toobtain reliable estimates of τrw-values and corresponding p-values. To examine ifmales were consistent in their behavior toward females across a female’s cycle, Imade similar matrix correlations via the same method using male solicitation oraggression rates of non-POP with the corresponding rates in POP.

To test whether females were overall more proceptive or resistant toward malesin non-POP or POP, I first averaged the proceptivity or resistance rates per femalefor all males in each estrous period. Subsequently, I compared the means perfemale for the 2 periods via Wilcoxon signed-ranks test. To compare if femaleproceptivity and resistance changed toward preferred and eschewed males duringthe estrous period —and female behavior has more evolutionary consequencesduring the fertile phase— I first averaged the proceptivity or resistance rates perfemale for each male category in POP and compared the corresponding dyads innon-POP via Wilcoxon signed-ranks tests (Fig. 1). Accordingly, I took theindividual males that were either preferred or eschewed in POP and compared thePOP mean with the mean of the same individual males —regardless if preferred oreschewed— in non-POP, e.g., applying proceptivity, for JO I averaged her POPpreferred males MS, LB, TU, SL, YB, and ST and compared the value with theaverage non-POP proceptivity rate of the same individual males (Table II).Corresponding analysis with male solicitation rates and male aggression ratestoward females served to investigate to which degree males influenced females intheir proceptivity and resistance behavior.

I performed the imputation procedure in Microsoft Office Excel 2003. I calculatedthe rowwise matrix correlations via MatMan (Noldus Information Technology2003). I estimated statistics based on 2000 permutations (de Vries et al. 1993). I

Female Mate Preferences of Pan troglodytes schweinfurthii 853

conducted all other statistical analyses via SPSS 12.0 for Windows. For theWilcoxon signed-ranks test my sample size was based on individual females (n = 6)and not on female-male dyads because dyads are not independent. The α-level ofsignificance is 0.05, and tests are 2-tailed.

Results

Expression of Female Mate Preferences

The expression of female mate preferences is exemplified in the preferred andeschewed male category. In contrast, if females did not express mate preferences,their proceptivity and resistance behavior was unbiased toward individual males andis exemplified in the neutral male category. For all females, more males are in thepreferred and eschewed category than in the neutral category throughout estrus(Table II). The only exception is TG: regarding proceptivity in non-POP, 60% of theindividual males are in the neutral male category. Further, regarding her resistancerates in POP, 50% of males are classified as neutral. For all other females, fewer thanone-third of individuals are in the neutral male category. Regarding proceptivity innon-POP, 5 of 6 females biased their behavior significantly (binomial tests, test

POP Eschewed Males

0

0.05

0.1

0.15

0.2

0.25

Non-POP POP

Pro

cept

ivit

y R

ate

A* POP Preferred Males

00.1

0.20.30.40.5

0.60.7

Non-POP POP

B*

0

0.2

0.4

0.6

0.8

1

1.2

Non-POP POP

Res

ista

nce

Rat

e

C

00.10.20.30.40.50.60.70.8

Non-POP POP

D*

Fig. 1 Average rates of female proceptivity (A, B) and female resistance (C, D) in the periovulatoryperiod (POP) and non-POP toward only the individual males that are eschewed or preferred in POP.Values for each female (n=6); high-fecund females (—•—) and low-fecund females (- - -○- - -).Significant difference between the 2 periods (*).

854 K. Pieta

proportion, 0.5: JO, p=0.000; OU, p=0.003; TG, p=0.754; NL, p=0.012; BR,p=0.000; LR, p=0.039; overall p=0.219), and regarding female resistance in non-POP, 4 of 6 females biased their behavior significantly. The 2 females that did not biastheir behavior significantly showed a trend to bias their behavior (binomial tests, testproportion, 0.5: JO, p=0.008; OU, p=0.006; TG, p=0.021; NL, p=0.070; BR,p=0.039; LR, p=0.065; overall p=0.688). Regarding proceptivity in POP, all 6females biased their behavior significantly (binomial tests, test proportion, 0.5: JO,p=0.000; OU, p=0.000; TG, p=0.004; NL, p=0.006; BR, p=0.000; LR, p=0.012;overall p=0.031), whereas with respect to resistance in POP, 3 of 6 females biasedtheir behavior significantly. Two of the 3 females that did not bias their behaviorsignificantly show a trend to bias their behavior (binomial tests, test proportion, 0.5:JO, p=0.008; OU, p=0.039; TG, p=1.000; NL, p=0.065; BR, p=0.002; LR,p=0.109; overall p=1.000). Overall, females biased their behavior toward individualmales much more than they acted unbiased (I obtained 18 p-values with a significantresult, 4 p-values with a trend to a significant result, and 2 p-values with anonsignificant result). Though females clearly expressed mate preferences with respectto proceptivity only during POP, generally most females expressed mate preferences innon-POP and POP, or at least showed a tendency to bias their behavior.

Consistency of Mate Preferences

I correlated non-POP rates (proceptivity, resistance, male solicitation, and maleaggression toward females) with the corresponding POP rates on a matrix level andsummarized all results (τrw- and p-values) in Table III. Female proceptivity rates didnot correlate significantly (for all females: τrw=0.07, pr=0.240). The same holds truefor female resistance rates. There is no significant correlation between resistancerates in non-POP with resistance rates in POP (for all females: τrw=0.11, pr=0.170).Overall, for females there is no consistency of mate preferences across estrus. Bycontrast, male solicitation rates toward females correlate positively (for all females:τrw=0.37, pr<0.001), indicating that the more a female was solicited by a male innon-POP, the more she was solicited by him in POP. The correlation is strongest forthe 3 high-fecund females (τrw=0.52, pr<0.001). Correlations regarding maleaggression rates between non-POP and POP for all females are nonsignificant(τrw=−0.03, pl=0.393), as well as for high-fecund females (τrw=0.14, pr=0.199).For low-fecund females there is a significant negative correlation (τrw=−0.28, pl=0.040), meaning that the more a female received aggression by a male in non-POP,the less she received aggression by him in POP. The results suggest that malesattempted to implement their preferences toward females via solicitation, but notaggression. Further, males were consistent in their mate preference across a female’scycle. In contrast, females were not consistent in their pattern of preference towardmales across their cycle.

Proceptivity and Resistance Differences Across Estrus

A comparison of proceptivity and resistance rates across estrus revealed nosignificant difference. Overall, females differed in neither their proceptivity rates(Wilcoxon signed-ranks test: Z=−0.314, n=6, p=0.753) nor resistance rates

Female Mate Preferences of Pan troglodytes schweinfurthii 855

(Z=−1.572, n=6, p=0.116) toward males between non-POP and POP. Further,females overall received no significantly higher rate of either male solicitation(Z=−1.572, n=6, p=0.116) or male aggression (Z=−0.314, n=6, p=0.753) ineither non-POP or POP.

POP Preferred and POP Eschewed Males

Females were substantially more proceptive toward POP eschewed males in non-POP (Wilcoxon signed-ranks test: Z=−2.201, n=6, p=0.028; Fig. 1A), andsubstantially less proceptive toward POP preferred males in non-POP (Z=−1.992,n=6, p=0.046; Fig. 1B). Though females did not differ significantly in theirresistance behavior across their cycle toward POP eschewed males (Z=−1.153, n=6,p=0.249; Fig. 1C), 5 of the 6 females showed far higher resistance to eschewedmales in POP than in non-POP, and only 1 female exhibited resistance in theopposite direction (Fig. 1C). Females resisted on average 70% of eschewed males’solicitations in POP vs. an average of 41% in non-POP. Perhaps the nonsignificantresult for Fig. 1C is a consequence of small sample size. Females were substantiallymore resistant toward POP preferred males in non-POP (Z=−2.023, n=6, p=0.043;Fig. 1D). Hence POP eschewed males were significantly less eschewed in non-POP,and POP preferred males were significantly more preferred in POP than in non-POP.Corresponding male behavior can account for no significant difference in femalepreferences. POP eschewed males neither solicited females significantly more in non-POP (proceptivity, Z=–1.782, n = 6, p=0.075; resistance, Z=–0.943, n=6, p=0.345),nor were they significantly more aggressive toward females in non-POP (proceptivity,Z=−1.363, n=6, p=0.173; resistance, Z=−0.405, n=6, p=0.686). Results for POPpreferred males were consistent. The females received neither significantly higher ratesof solicitation (proceptivity, Z=−1.782, n=6, p=0.075; resistance, Z=−0.943, n=6, p=0.345) nor aggression (proceptivity, Z=−0.105, n=6, p=0.917; resistance, Z=−1.214,n=6, p=0.225) by the POP preferred males during non-POP. Thus Kanyawara femalesseem to mate selectively during POP. On closer examination, there is a trend for bothpreferred and eschewed males based on proceptivity to solicit females more in POPthan in non-POP. Though this could have influenced female proceptivity behaviortoward males to some extent, it does not explain the whole magnitude of their mateselectivity during POP. Though it appears that male solicitation might have had agreater influence on female mating preferences than male aggression toward females,overall one cannot explain female mate selectivity during the fertile phase by eithermale solicitation or their aggression toward females.

Discussion

My results indicate that 1) Kanyawara female chimpanzees expressed matepreferences toward particular males and 2) the mate preferences differed duringfertile vs. nonfertile estrus.

Females did not randomly exhibit proceptive or resistance behavior toward males.Though TG somewhat fit the picture of behaving randomly toward males before apossible copulation according to proceptivity in non-POP and resistance in POP, the

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other females did not. The 5 females clearly had mating preferences toward certainmales across their estrus.

Researchers found similar results for the expression of female mating preferencesamong other East African chimpanzees. Matsumoto-Oda (1999) described femalechimpanzees in Mahale copulating promiscuously, but not randomly. Tutin (1979)investigated partner preferences via copulation rates with an arbitrary index forfemale and male chimpanzees in Gombe. Of the 81 dyads, 34 showed indices ofpartner preferences, 14 positive and 20 negative. None of the 7 females and only 2 ofthe 18 males showed no index of preference. Therefore, Tutin concluded that theopportunistic mating pattern is not totally indiscriminative. While Tutin couldexplain little about individual preferences, she found that primary kin showednegative indices. Sexual activity is infrequent between maternal siblings andbetween mothers and sons (Pusey 1980). Consequently, kinship could also influencethe expression of mate preferences. Owing to the lack of genetic information, I couldnot determine to what degree kinship influenced mating preferences, i.e., resistancebehavior to avoid inbreeding. The only 2 dyads of maternal siblings to myknowledge were LR-LK, and LR-AJ (Wrangham, unpub. data). LR eschewed hermaternal brother LK more than her older maternal brother AJ. Because LK was ca. 7yr old by the time LR was born, and AJ was about to reach adulthood, LR muchmore associated with her younger brother, and thus might have been more inhibitedto copulate with LK by the time she became sexually active (cf. Pusey 1980).

My results on female mate preferences (Table II) are directly comparable toStumpf’s (2004) findings on West African chimpanzees in Taï, where sheinvestigated mate preferences of 11 parous females with 4 males in the community(South group), and 3 parous females with 3 males in another community (Northgroup). Stumpf (2004) demonstrated that out of 13 parous females in non-POP onlyfor 3 females the majority of males were neutral according to proceptivity rates, andonly for 1 female they were neutral according to resistance rates. In POP, accordingto proceptivity, for none of 9 Taï females were more than one-third of the malesneutral, and concerning resistance rates, for 10 Taï females males were neutral foronly 1 of them. In brief, for Taï females a smaller proportion of males were neutral inPOP than in non-POP, whereas in Kanyawara females the small proportion ofcategorized neutral males was distributed evenly in both phases; i.e., both Taï andKanyawara females expressed mating preferences. However, Taï females hadstronger mate preferences in POP than in non-POP, while Kanyawara females hadstrong mate preferences in both non-POP and POP. Though the stronger matepreferences during POP vs. the rest of the estrous period of Taï females seem toreflect their selective mating strategy during the fertile phase (Stumpf and Boesch2005), the Kanyawara females’ expression of strong mate preferences across estrusseem to reflect a reproductive strategy to confuse paternity on closer examination.That is, females solicited different males for mating in non-POP than in POP, andresisted different soliciting males, respectively. Thus, the inconsistency in preferredand eschewed males across estrus suggests a shift in mate preferences between non-POP and POP, indicating that Kanyawara females seem to use a mixed reproductivestrategy: besides mating selectively during POP (Fig. 1), they prefer different matingpartners during non-POP and POP to mate in a promiscuous manner, possibly toconfuse paternity to avoid infanticide (cf. van Schaik et al. 2000). The strategy is

Female Mate Preferences of Pan troglodytes schweinfurthii 857

feasible because infanticide poses a risk for chimpanzee mothers (Arcadi andWrangham 1999; Boesch and Boesch-Achermann 2000; Watts 2007). However, theshift in mate preference seems to be a general female tactic, which both parousfemales and females that are less fecund, such as postpartum or nulliparous females,adopt. The tactic may allow females to deceive males for reasons of paternityconfusion, indicating that promiscuity among females is more strategic thanpreviously thought. The only other species to display such a shift in female matingpreferences across the reproductive cycle is Homo sapiens. Various studies indicatethat women systematically vary their mate preferences across their menstrual cycles(Gangestad et al. 2004; Penton-Voak et al. 1999; Rikowski and Grammer 1999;Thornhill and Gangestad 1999). Though the studies were able to associate femalepreferences with certain male attributes, I cannot explain which male attributesattracted Kanyawara focal females.

One cannot directly compare female consistency of mate preferences across estrusbetween Kanyawara and Taï because matrix correlations for Taï females were notpossible (matrices require more columns, i.e., more males). However, Taï femaleswere also not consistent in their mate preferences across estrus because individualmales could change the preferred, neutral, or eschewed category between non-POPand POP (Stumpf 2004).

As the females’ reproductive strategy was reflected in their inconsistency of matepreferences across estrus, the males’ reproductive strategy was characterized by itsconsistency of mate preferences in non-POP and POP. The more a male solicited acertain female for mating in non-POP, the more he solicited her in POP, particularlythe 3 parous females (cf. Emery Thompson and Wrangham 2008). Adult males findolder, parous females more attractive than younger, nulliparous females (Goodall1986; Muller et al. 2006; Tutin 1979), which have a reduced probability ofconception (Wrangham 2002). The male tendency to solicit parous females moreoften during POP will heighten their reproductive success because the likelihood offertilization is greatest. Male solicitation also seemed to be more important forimplementing their preferences toward certain females than the use of aggressiontoward females across their estrus, because aggression rates did not correlatebetween non-POP and POP, or even correlated negatively for low-fecund females.

Certainly, one might argue that females shifted their mate preferences acrossestrus not intentionally but instead were influenced by male mating effort, explicitlymale solicitation. For example, if a female solicits a certain male in non-POP, shedoes not necessarily solicit him in POP, because instead he is soliciting her at anyrate and often is more willing to mate with her in POP. The argument does not seemconvincing for the following reasons: 1) If female mate preferences would have beenjust a reflection of male solicitation effort, they would have had either to eschew orto prefer all males in POP similarly because all males —preferred and eschewed—tended to solicit them more in POP. 2) Females changed their preferences across theestrous phases not only with regard to proceptive behavior but also with regard toresistance toward soliciting males.

Though overall proceptivity of Kanyawara females toward males did not differbetween the 2 estrous phases, Stumpf and Boesch’s (2005) findings were different.Taï females were significantly more proceptive in non-POP, when conception wasnot likely. The more promiscuous mating strategy in non-POP allows Taï females to

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mate for nonreproductive reasons, such as paternity confusion. Another benefitStumpf and Boesch (2005) suggested was a possible way for females to stimulatemale-male competition to mate with the more superior males later in POP. Unlike Taïfemales, Kanyawara females did not seem to follow a strategy to induce male-malecompetition via increased overall proceptive behavior toward them specifically innon-POP. However, Kanyawara males increase male-male competition during fertileperiods of females (Muller and Wrangham 2004).

Kanyawara females did not overall resist males more in either phase of theircycles. In contrast, female Taï chimpanzees were significantly more resistant towardmales in POP. Thus, they were more selective during POP and more promiscuousoutside POP, suggesting that Taï females may use a mixed reproductive strategy. Bymating selectively during POP, Taï females may attempt to influence which malessire their offspring because conception is likely (Stumpf and Boesch 2005).Researchers conceived a similar interpretation for female chimpanzees in Mahale.Matsumoto-Oda (1999) reported that females utilize 2 mating strategies at differentstages of estrus: a multimale strategy outside the periovulatory period, and a best-male strategy when they are fertile. Given that high-ranking males tended to matewith females during POP significantly more often than low-ranking males do(Nishida 1997), Matsumoto-Oda suggested that females adopt the best-male strategywhen they are more likely to conceive.

The rather tactical promiscuity of Kanyawara females —expressed in the females’shift in mate preferences across estrus— revealed another scenario when looking atthe subset of males. Kanyawara females endeavored mating selectively during thefertile phase, and thus seem to have adopted a selective reproductive strategy duringPOP. Consequently, Kanyawara females appear to have a mixed reproductivestrategy, similar to that of Taï and Mahale female chimpanzees. When examiningpreferred and eschewed males and changes in proceptivity and resistance across thefemale cycle, I noted a clearer pattern for preferred males than for eschewed males.Females were more proceptive and less resistant toward preferred males in POP thanin non-POP. This is interesting insofar as the results are directly comparable to themethod of analysis of Stumpf and Boesch (2005), who did not find this pattern. Taïfemales were highly proceptive and not resistant toward preferred males in POP aswell as in non-POP. It seems that they simply had no reason not to mate with POPpreferred males outside of POP (Stumpf and Boesch 2005). However, Stumpf andBoesch (2005) noted a clear pattern for eschewed males. Taï females were moreresistant and less proceptive toward eschewed males in POP than in non-POP.Because for all 8 Taï females sufficient data were available from resisted eschewedmales more in POP than in non-POP (Stumpf and Boesch 2005), Taï femalesapparently are able to resist eschewed males more effectively than Kanyawarafemales can. The finding, and Taï female ability to be highly proceptive and notresistant toward preferred males throughout estrus, are probably due to a variety ofsocial factors and ecological constraints such as fewer males in the community(Stumpf and Boesch 2005), female-female friendships (Boesch and Boesch-Achermann 2000), greater cohesiveness (Lehmann and Boesch 2004), higher femalesociality (Lehmann and Boesch 2008), and a lower cost of grouping and thus lowersexual coercion (Wrangham 2002) vs. other —particularly East African— chimpanzeecommunities.

Female Mate Preferences of Pan troglodytes schweinfurthii 859

Though Kanyawara females resisted eschewed males not significantly more inPOP than in non-POP, it seems clear that females can and do resist males in thefertile phase. Only 1 of 6 females did not resist eschewed males more in POP vs.non-POP and they resisted soliciting eschewed males at a very high rate, i.e., 70% inPOP vs. 41% in non-POP. Further, females solicited eschewed males more formating during non-POP than during POP. The tactic allows females to mate fornonreproductive reasons such as paternity confusion. Moreover, Kanyawara femalesdecreased resistance toward soliciting preferred males and increased proceptivitytoward preferred males during POP vs. non-POP. The strategy seems biologicallymeaningful because females would presumably want preferred males to father theiroffspring. My data support the conclusion that Kanyawara females appear to changetheir mating strategies and selectivity during estrus.

One objection could be that female mate selectivity during POP might have beeninduced by male mating strategies because high-ranking males maintain highermating access during POP than low-ranking males do (Muller and Mitani 2005), orsome males might have had more knowledge about a female’s fertilization potentialthan others did. Moreover, females could have anticipated male coercion and simplysolicited males for copulation or conceded to a soliciting male before they becomeaggressive. My results show no significant difference of preferred and eschewedmale solicitation rates between the 2 estrous phases; still, there is a trend of bothpreferred and eschewed males with regard to proceptivity to solicit females forcopulation more in POP than in non-POP (cf. Emery Thompson and Wrangham2008). Thus, if females would have consented to soliciting males, females wouldhave had to be either significantly more proceptive toward preferred and eschewedmales, e.g., because they fear male punishment for not wanting to mate with them, orsignificantly less proceptive toward preferred and eschewed males, e.g., because allmales are nevertheless soliciting them at higher rates, or behave randomly. However,females adjusted their proceptive behavior toward preferred and eschewed males to fitthe biologically meaningful picture of mating selectively, i.e., attempting to mate withpreferred males in POP and attempting not to mate with eschewedmales in POP, insteadof to comply with male solicitation efforts. Consequently, male solicitation or maleaggression toward females could not account for female mate selectivity during thefertile phase. Kanyawara females seem to have adopted a selective reproductive matingstrategy despite increased male solicitation (cf. Emery Thompson and Wrangham2008), male-male competition (Muller and Wrangham 2004), and male coercion(Muller et al. 2007) during the fertile period.

I cannot completely rule out the possibility that owing to the lack of hormonaldata I did not always pinpoint the fertile period exactly, which may weaken myresults. Nevertheless, the majority of studies on wild chimpanzees rely on behavioralinstead of hormonal data. Because my sample size of females is small, one needs tointerpret my findings in some ways with caution. But a small sample size onlydecreases statistical power, which means it is more likely not to find significantdifferences, when in fact the differences would be significant (cf. Cohen 1988).Further, I had much more data on cycles of low-fecund vs. high-fecund females,which could have affected the outcome of my results. However, the number ofindividuals of the 2 subsets of females was evenly distributed. Hence, my resultssuggest that the pattern of changing mating strategies and selectivity during estrus is

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a general female chimpanzee trait in Kanyawara, and not specifically a trait of high-fecund females that are under more prominent reproductive constraints vs. low-fecund females. The trait may serve females consequently to obscure paternity, yetmate selectively with preferred males during the fertile period, and thus may act ascounter-adaption to male mating strategies. This mixed sexual —and consequentlyreproductive— strategy is similar to that reported for Taï (Stumpf and Boesch 2005)and Mahale females (Matsumoto-Oda 1999).

Acknowledgments I thank the Uganda National Council for Science and Technology, the Uganda WildlifeAuthority, and the Makerere University Biological Field Station for permission to conduct this research,especially Gilbert Isabirye-Basuta and John Kasenene. I thank Richard Wrangham for inviting me to studychimpanzees at Kanyawara, for his guidance and his constant encouragement. I also thank Karl Grammer forsupervising my study and for his support and enthusiasm. For tracking chimpanzees and long working hours,I thank the late Barwogeza John, Katongole Christopher, Mugurusi Francis, the late Muruuli Christopher, thelate Muhangyi Donor, and Tuhairwe Peter. Thanks go to Charlotte Hemelrijk, who kindly pointed out mymissing value problem in social matrices, and Han de Vries, who solved the problem with great enthusiasm. Iacknowledge Max Kauer for his help to untangle a statistical knot. Further, I thank Melissa Emery Thompsonand Rebecca Stumpf for inviting me to the IPS Symposium. Additional thanks go to Thomas Bodendorfer,Kim Duffy, Melissa Emery Thompson, Christine Hrubesch, Marianne Imhof, Martin Muller, AmyPokempner, and Signe Preuschoft for comments and discussions on the manuscript. The Bureau forInternational Studies, University of Vienna, and the Österreichische Forschungsgemeinde provided financialsupport. Finally, I thank Rebecca Stumpf and reviewers for very helpful comments of an earlier version of themanuscript, which greatly improved it.

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