Variation in maternal care - Between species - Within species Parent-offspring conflict Mothering Cercopithecines Baboon mother and infant

ParkRide Carried Cling Nest Tree Variation between species Style (park/ride) The main mammal pattern (rodents, pigs, ungulates, etc)

Park (nest, branch) Park + Ride Ride Ancestral state unknown Ross (2001) IJP Tarsius Ceboids Cercopithecoids Human Apes Daubentonia Indriidae Lepilemur Tree-shrews Loris Lorisoids Galago/oides Euoticus, Otolemur Mouse lemurs Phaner Varecia Lemur Hapalemur Eulemur 1. Ancestral state = Parking 2. Riding evolved often 3. Riding is maintained Riding is a repeated primate trait.

Park (nest, branch) Park + Ride Ride Ancestral state unknown Ross (2001) IJP Tarsius Daubentonia Indriidae Lepilemur Tree-shrews Loris Lorisoids Galago/oides Euoticus, Otolemur Mouse lemurs Phaner Varecia Hapalemur Apes Cercopithecoids Ceboids Lemur Eulemur Riding: > 4 independent appearances

Park (nest, branch) Park + Ride Ride Ancestral state unknown Ross (2001) IJP Tarsius Ceboids Cercopithecoids Apes Daubentonia Indriidae Lepilemur Tree-shrews Loris Galago/oides Mouse lemurs Varecia Lemur Hapalemur Human Lorisoids Euoticus, Otolemur Phaner Park+Ride: > 2 from Park* > 1 from Ride + * * +

Costs (allometric) of riding, cf. parking: (1) Smaller home ranges (2) Late weaning (3) Late age of first reproduction Riding compared to parking: (1) Same Inter-birth interval (2) Same Growth rate (3) Same Infant size (4) Same Brain size Retrieving parked infant Arctocebus So why has riding evolved? H o : Improved infant survival Ross (2001) IJP

Riders: Contact time similar in different species

Mothers carry offspring more when needed Altmann & Samuels 1992 BES Kanyawara Field Station (Photo AH)

Mothers are important for survival!

… even when not dead

Mothers are important for RS! Large group Small group

Variation within species 1. Ecological conditions: Food availability Gilgil Amboseli Drakensberg High-quality Low-quality % time spent feeding by mother ………… Expected Observed

Lycett et al 1998 BES P. c. ursinus Chacma Harsh conditions: Infants forage less independently (closer to mother) Age % Time Good habitat Intermediate habitat Bad habitat Twice more independent in a good habitat compared to a bad one !

Lycett et al 1998 BES P. c. ursinus Chacma Drakensburg Harsh conditions: In harsh environment, mothers work harder. (infants suckle more) { 5x diff. Good habitat Intermediate habitat Bad habitat

Variation within species Ecological conditions: Predation Risk No predation Some predn Mother’s hard work pays!

Variation in maternal care 3. Dominance rank / style High-rank mothers carried less.

Mother’s Style Laissez-faireRestrictive Mother’s rankHighLow Infant allowed to leave< 2 monthsLater M follows IRareCommon M joins IRareCommon M punishes ILessMore M-I contactLessMore Altmann (1980)

Variation in maternal care Maternal style

Parent-Offspring conflict: OBSERVER’S Perspective B = Benefit to Offspring (e.g. 10 cc of milk) C = Cost to Mother (e.g. extra days before next birth) Age of Offspring B/CB/C WEANING CONFLICT AGREED: M CARES AGREED: M STOPS B=CB=C

When to wean? MOTHER’S Perspective B/2 = Benefit to Mother ? ? ? B = Benefit to Offspring C = Cost to Mother Age of Offspring B/CB/C Wean when “rB < C” i.e. when B/2 < C

C/2 = Cost to Offspring When to wean? OFFSPRING’S Perspective B = Benefit to Offspring (e.g. 10 cc of milk) C = Cost to Mother Age of Offspring B/CB/C Wean when “B < rC” i.e. when B < C/2

Wean when “B < rC” i.e. when B < C/2 C/2 B Age of Offspring B/2 C Age of Offspring Wean when “rB < C” i.e. when B/2 < C “EARLY!!” “LATE!!” CONFLICT!!! WHY PARENTS AND CHILDREN FIGHT

Parent-offspring conflict Infant age (weeks) Cayo Santiago (feral, subtropic) Madingley (cages, UK) % total nipple contacts (attempted + successful) rejected by mother Mothers do reject young

Infant age (weeks) Relative Responsibility Index: RRI RRI = (% M-I body contacts initiated by infant) - (% M-I body contacts terminated by infant) RRI I joins and/or M leaves M joins and/or I leaves Who’s responsible for declining maternal investment? Mother’s investment falls

Gelada: More infant contact during RESTING SOCIALIZING than during FEEDING MOVING Contact MOTHER Contact NIPPLE Infants seek investment mostly when mother is not busy

Gelada: Rejections occur almost entirely when mother is feeding No rejections were observed during moving and resting

Time on nipple Ventral + Nipple Suckling time decreases little!

van Schaik & van Noordwijk (1999) Primates Mothers need to wean early to increase their lifetime RS Age-specific fecundity Macaques (3 species)

Parent-offspring conflict: Amount versus Timing Barrett et al 1995 Anim Behav

Play Fighting Allomothering Learning Juvenile relationships Childhood in Macaques Macaca fuscata Japanese macaque

Benefits of Play: cf. going to school Benefit to young: Skills? Lone playM = F Play-fightingM > FNHP’s Play-motherF > MNHPs’ Tool-useF > MTai, Gombe Social manipulation? Mother distracting Infant (weaning) Learning competition Early coalitions/relationships?

Benefits of Play: cf. going to school Lone playM = F

Benefits of Play: cf. going to school Play-motherF > MNHPs’

Benefits of Play: cf. going to school Play-fightingM > FNHP’s

Benefits of Play: cf. going to school Tool-useF > MTai, Gombe

Rainfall % play-time Economics of play (1) Benefit More play when more food Some primates never play!

Economics of play (2) Cost Vervets eaten when playing – Red-tailed infant playing at the very top of a fruit tree (Kibale)  caught by eagle

Vervet allomothers (captive) Who? Juvenile ff65 (sibs; high-rank) Adult ff25 Juvenile mm 7 Adult mm 3 Benefit to mother

Why be an alloparent? Females - nulliparous *** Practice: improved mothering ** Nepotism: caring for kin * Market forces: care for HR’s offspring (get support in return) Females - parous (e.g. langurs) * Nepotism * Non-kin: odd suggesting friendship? Males - juvenile * Nepotism * Practice mating * Market forces: care for HR’s offspring (get support in return) Males - adult ** Paternal care *** Mating effort

Wallen et al. (1995) Hormones and Behavior Daughter Son Yearling- controlled proximity to mother (% time) Girls spend more time with mother than boys Rhesus macaque

Wallen et al. (1995) Hormones and Behavior Daughter Sons Yearling- controlled proximity to mother (% time) Neonatal T affects how much time boys spend with mother T control TT Rhesus macaque

Lonsdorf et al 2004 Nature % time at mound spent termite-fishing: girls > boys

Termites per dip Lonsdorf et al 2004 Nature

Mother’s % dips at given tool length Daughter’s % dips at given tool length Lonsdorf et al 2004 Nature

Mother’s % dips at given tool length Son’s % dips at given tool length

Juvenile relationships: anticipating adulthood Dominance relations in FB-groups Juv F Juv M Juv FMaternal RankSize Juv MSizeSize e.g. Pereira, Amboseli baboons

Juvenile relationships: anticipating adulthood Infant Juvenile Adult Pereira, Amboseli baboons 030(months)60 # Supplants received per hour from HR females Female Male

Juvenile relationships: anticipating adulthood Juv F Juv M Challenged by Adult FFYESNO Supported by Adult FFYESNO ‘Head-flag’ to Adult FFYESNO ““ Adult MM NOYES Non-kin supportedHR-FFJuv MM Pereira, Amboseli baboons

Baboon rules for treating juveniles Adult FF Juvenile FF:support their rank (winner support) Juvenile MM: dominate as long as possible Adult MM Ignore sex/rank (dominate all) Support possible offspring

Old viewNew view JuvenilePassiveActive Juv periodLong, to learnFast growth, risky Major influencesProximateUltimate (experience)(social system) Quality of lifeRelaxedDangerous (>50% die)

23 FF, 2 groups, 240 cases 90% held I’s = higher-rank F > M Kin > Unrelated De Waal 1990 Primates “Double-holding”:

Play Play partners InfantsSame size HR preferred Juv FFInfants (HR preferred)Juv MM